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1.  Topography of connections between human prefrontal cortex and mediodorsal thalamus studied with diffusion tractography 
Neuroimage  2010;51(2):555-564.
Studies in monkeys show clear anatomical and functional distinctions among networks connecting with subregions within the prefrontal cortex. Three such networks are centered on lateral orbitofrontal cortex, medial frontal and cingulate cortex, and lateral prefrontal cortex and all have been identified with distinct cognitive roles. Although these areas differ in a number of their cortical connections, some of the first anatomical evidence for these networks came from tracer studies demonstrating their distinct patterns of connectivity with the mediodorsal (MD) nucleus of the thalamus. Here, we present evidence for a similar topography of MD thalamus prefrontal connections, using non-invasive imaging and diffusion tractography (DWI–DT) in human and macaque. DWI–DT suggested that there was a high probability of interconnection between medial MD and lateral orbitofrontal cortex, between caudodorsal MD and medial frontal/cingulate cortex, and between lateral MD and lateral prefrontal cortex, in both species. Within the lateral prefrontal cortex a dorsolateral region (the principal sulcus in the macaque and middle frontal gyrus in the human) was found to have a high probability of interconnection with the MD region between the regions with a high probability of interconnection with other parts of the lateral prefrontal cortex and with the lateral orbitofrontal cortex. In addition to suggesting that the thalamic connectivity in the macaque is a good guide to human prefrontal cortex, and therefore that there are likely to be similarities in the cognitive roles played by the prefrontal areas in both species, the present results are also the first to provide insight into the topography of projections of an individual thalamic nucleus in the human brain.
doi:10.1016/j.neuroimage.2010.02.062
PMCID: PMC2877805  PMID: 20206702
Anatomy; DTI; Human; Macaque; Thalamus
2.  Performance Monitoring Local Field Potentials in the Medial Frontal Cortex of Primates: Anterior Cingulate Cortex 
Journal of neurophysiology  2007;99(2):759-772.
We describe intracranial local field potentials (LFP) recorded in the anterior cingulate cortex (ACC) of macaque monkeys performing a saccade countermanding task. The most prominent feature at ∼70% of sites was greater negative polarity after errors than after rewarded correct trials. This negative polarity was also evoked in unrewarded correct trials. The LFP evoked by the visual target was much less polarized, and the weak presaccadic modulation was insufficient to control the initiation of saccades. When saccades were cancelled, LFP modulation decreased slightly with the magnitude of response conflict that corresponds to the coactivation of gaze-shifting and -holding neurons estimated from the probability of canceling. However, response time adjustments on subsequent trials were not correlated with LFP polarity on individual trials. The results provide clear evidence that error- and feedback-related, but not conflict-related, signals are carried by the LFP in the macaque ACC. Finding performance monitoring field potentials in the ACC of macaque monkeys establishes a bridge between event-related potential and functional brain-imaging studies in humans and neurophysiology studies in non-human primates.
doi:10.1152/jn.00896.2006
PMCID: PMC2675936  PMID: 18077665
3.  Localized Microstimulation of Primate Pregenual Cingulate Cortex Induces Negative Decision-Making 
Nature Neuroscience  2012;15(5):776-785.
The pregenual anterior cingulate cortex (pACC) has been implicated in human anxiety disorders and depression, but the circuit-level mechanisms underlying these disorders are unclear. We took as a clue evidence that in healthy individuals, the pACC is involved in cost-benefit evaluation. We developed a macaque version of an approach-avoidance decision task used to evaluate anxiety and depression in humans and, with multi-electrode recording and cortical microstimulation, we probed pACC function as monkeys performed this task. We found that the macaque pACC has an opponent-process like organization of neurons representing motivationally positive and negative subjective value. These two neuronal populations overlapped spatially, except in one pACC subzone, where neurons with negative coding were more numerous. Strikingly, microstimulation in this subzone, but not elsewhere in the pACC, increased negative decision-making, and this negative biasing was blocked by anti-anxiety drug treatment. This cortical zone could be critical for regulating negative emotional valence and anxiety in decision-making.
doi:10.1038/nn.3088
PMCID: PMC3369110  PMID: 22484571
4.  Functional Imaging Reveals Numerous Fields in the Monkey Auditory Cortex 
PLoS Biology  2006;4(7):e215.
Anatomical studies propose that the primate auditory cortex contains more fields than have actually been functionally confirmed or described. Spatially resolved functional magnetic resonance imaging (fMRI) with carefully designed acoustical stimulation could be ideally suited to extend our understanding of the processing within these fields. However, after numerous experiments in humans, many auditory fields remain poorly characterized. Imaging the macaque monkey is of particular interest as these species have a richer set of anatomical and neurophysiological data to clarify the source of the imaged activity. We functionally mapped the auditory cortex of behaving and of anesthetized macaque monkeys with high resolution fMRI. By optimizing our imaging and stimulation procedures, we obtained robust activity throughout auditory cortex using tonal and band-passed noise sounds. Then, by varying the frequency content of the sounds, spatially specific activity patterns were observed over this region. As a result, the activity patterns could be assigned to many auditory cortical fields, including those whose functional properties were previously undescribed. The results provide an extensive functional tessellation of the macaque auditory cortex and suggest that 11 fields contain neurons tuned for the frequency of sounds. This study provides functional support for a model where three fields in primary auditory cortex are surrounded by eight neighboring “belt” fields in non-primary auditory cortex. The findings can now guide neurophysiological recordings in the monkey to expand our understanding of the processing within these fields. Additionally, this work will improve fMRI investigations of the human auditory cortex.
High-resolution fMRI reveals a detailed functional description of auditory cortical fields in the macaque monkey.
doi:10.1371/journal.pbio.0040215
PMCID: PMC1479693  PMID: 16774452
5.  Visual Field Map Clusters in Macaque Extrastriate Visual Cortex 
The macaque visual cortex contains more than 30 different functional visual areas, yet surprisingly little is known about the underlying organizational principles that structure its components into a complete ‘visual’ unit. A recent model of visual cortical organization in humans suggests that visual field maps are organized as clusters. Clusters minimize axonal connections between individual field maps that represent common visual percepts, with different clusters thought to carry out different functions. Experimental support for this hypothesis, however, is lacking in macaques, leaving open the question of whether it is unique to humans or a more general model for primate vision. Here we show, using high-resolution BOLD fMRI data in the awake monkey at 7 Tesla, that area MT/V5 and its neighbors are organized as a cluster with a common foveal representation and a circular eccentricity map. This novel view on the functional topography of area MT/V5 and satellites indicates that field map clusters are evolutionarily preserved and may be a fundamental organizational principle of the old world primate visual cortex.
doi:10.1523/JNEUROSCI.0518-09.2009
PMCID: PMC2749229  PMID: 19474330
extrastriate cortex; MT/V5; Macaque; retinotopy; fMRI; 7T
6.  Cytology and Functionally Correlated Circuits of Human Posterior Cingulate Areas 
NeuroImage  2005;29(2):452-466.
Human posterior cingulate cortex (PCC) and retrosplenial cortex (RSC) form the posterior cingulate gyrus, however, monkey connection and human imaging studies suggest that PCC area 23 is not uniform and atlases mislocate RSC. We histologically assessed these regions in 6 postmortem cases, plotted a flat map, and characterized differences in dorsal (d) and ventral (v) area 23. Subsequently, functional connectivity of histologically guided regions of interest (ROI) were assessed in 163 [18F]fluorodeoxyglucose human cases with PET. Compared to area d23, area v23 had a higher density and larger pyramids in layers II, IIIc, and Vb and more intermediate neurofilament-expressing neurons in layer Va. Coregisrtration of each case to standard coordinates showed that the ventral branch of the splenial sulci coincided with the border between d/v PCC at −5.4±0.17 cm from the vertical plane and +1.97±0.08 cm from the bi-commissural line. Correlation analysis of glucose metabolism using histologically guided ROIs suggested important circuit differences including dorsal and ventral visual stream inputs, interactions between the vPCC and subgenual cingulate cortex, and preferential relations between dPCC and the cingulate motor region. The RSC, in contrast, had restricted correlated activity with pericallosal cortex and thalamus. Visual information may be processed with an orbitofrontal link for synthesis of signals to drive premotor activity through dPCC. Review of the literature in terms of a PCC duality suggests that interactions of dPCC, including area 23d, orients the body in space via the cingulate motor areas, while vPCC interacts with subgenual cortex to process self-relevant emotional and non-emotional information and objects and self reflection.
doi:10.1016/j.neuroimage.2005.07.048
PMCID: PMC2649771  PMID: 16140550
Cingulate cortex; cytoarchitecture; retrosplenial cortex; neurofilament proteins; glucose metabolism; cerebral cortex; self reflection
7.  Cognition and medial frontal cortex in health and disease 
Current opinion in neurology  2006;19(6):586-592.
Purpose of review
Recent work on the role of medial frontal cortex in cognition and its involvement in neurological disorders is critically reviewed.
Recent findings
The highly influential notion of conflict monitoring by the anterior cingulate has been called into question by monkey single-cell neurophysiology and lesion studies in monkeys and humans. An alternative role for this region in adapting behaviour in response to changing demands over time is gaining support. By contrast, the more dorsally placed pre-supplementary motor area and supplementary eye field have been implicated in direct executive control in situations of response conflict. Although more rostral medial areas have been linked to complex cognitive operations involving references to the self, conceptual obstacles make the evidence difficult to interpret. The role of orbitofrontal cortex in guiding action based on value has been reinforced.
Summary
This area continues to generate both interest and controversy. A few striking discrepancies between data from functional imaging and interventional techniques illustrate the hazards of drawing strong conclusions from merely correlative evidence. More broadly, a case can be made for tempering the empirical enthusiasm here with a little more theoretical restraint.
doi:10.1097/01.wco.0000247609.36482.ae
PMCID: PMC2658463  PMID: 17102698
medial frontal cortex; cingulate cortex; pre-supplementary motor area; supplementary eye field; orbitofrontal cortex; ventromedial cortex
8.  The Organization of Dorsal Frontal Cortex in Humans and Macaques 
The Journal of Neuroscience  2013;33(30):12255-12274.
The human dorsal frontal cortex has been associated with the most sophisticated aspects of cognition, including those that are thought to be especially refined in humans. Here we used diffusion-weighted magnetic resonance imaging (DW-MRI) and functional MRI (fMRI) in humans and macaques to infer and compare the organization of dorsal frontal cortex in the two species. Using DW-MRI tractography-based parcellation, we identified 10 dorsal frontal regions lying between the human inferior frontal sulcus and cingulate cortex. Patterns of functional coupling between each area and the rest of the brain were then estimated with fMRI and compared with functional coupling patterns in macaques. Areas in human medial frontal cortex, including areas associated with high-level social cognitive processes such as theory of mind, showed a surprising degree of similarity in their functional coupling patterns with the frontal pole, medial prefrontal, and dorsal prefrontal convexity in the macaque. We failed to find evidence for “new” regions in human medial frontal cortex. On the lateral surface, comparison of functional coupling patterns suggested correspondences in anatomical organization distinct from those that are widely assumed. A human region sometimes referred to as lateral frontal pole more closely resembled area 46, rather than the frontal pole, of the macaque. Overall the pattern of results suggest important similarities in frontal cortex organization in humans and other primates, even in the case of regions thought to carry out uniquely human functions. The patterns of interspecies correspondences are not, however, always those that are widely assumed.
doi:10.1523/JNEUROSCI.5108-12.2013
PMCID: PMC3744647  PMID: 23884933
9.  Molecular Evidence for Distinct Genotypes of Monkey B Virus (Herpesvirus Simiae) Which Are Related to the Macaque Host Species 
Journal of Virology  1998;72(11):9224-9232.
Although monkey B virus (herpesvirus simiae; BV) is common in all macaque species, fatal human infections appear to be associated with exposure to rhesus macaques (Macaca mulatta), suggesting that BV isolates from rhesus monkeys may be more lethal to nonmacaques than are BV strains indigenous to other macaque species. To determine if significant differences that would support this supposition exist among BV isolates, we compared multiple BV strains isolated from rhesus, cynomolgus, pigtail, and Japanese macaques. Antigenic analyses indicated that while the isolates were very closely related to one another, there are some antigenic determinants that are specific to BV isolates from different macaque species. Restriction enzyme digest patterns of viral DNA revealed marked similarities between rhesus and Japanese macaque isolates, while pigtail and cynomolgus macaque isolates had distinctive cleavage patterns. To further compare genetic diversity among BV isolates, DNA sequences from two regions of the viral genome containing genes that are conserved (UL27 and US6) and variable (US4 and US5) among primate alphaherpesviruses, as well as from two noncoding intergenic regions, were determined. From these sequence data and a phylogenetic analysis of them it was evident that while all isolates were closely related strains of BV, there were three distinct genotypes. The three BV genotypes were directly related to the macaque species of origin and were composed of (i) isolates from rhesus and Japanese macaques, (ii) cynomolgus monkey isolates, and (iii) isolates from pigtail macaques. This study demonstrates the existence of different BV genotypes which are related to the macaque host species and thus provides a molecular basis for the possible existence of BV isolates which vary in their levels of pathogenicity for nonmacaque species.
PMCID: PMC110342  PMID: 9765470
10.  Value and Prediction Error in Medial Frontal Cortex: Integrating the Single-Unit and Systems Levels of Analysis 
The role of the anterior cingulate cortex (ACC) in cognition has been extensively investigated with several techniques, including single-unit recordings in rodents and monkeys and EEG and fMRI in humans. This has generated a rich set of data and points of view. Important theoretical functions proposed for ACC are value estimation, error detection, error-likelihood estimation, conflict monitoring, and estimation of reward volatility. A unified view is lacking at this time, however. Here we propose that online value estimation could be the key function underlying these diverse data. This is instantiated in the reward value and prediction model (RVPM). The model contains units coding for the value of cues (stimuli or actions) and units coding for the differences between such values and the actual reward (prediction errors). We exposed the model to typical experimental paradigms from single-unit, EEG, and fMRI research to compare its overall behavior with the data from these studies. The model reproduced the ACC behavior of previous single-unit, EEG, and fMRI studies on reward processing, error processing, conflict monitoring, error-likelihood estimation, and volatility estimation, unifying the interpretations of the role performed by the ACC in some aspects of cognition.
doi:10.3389/fnhum.2011.00075
PMCID: PMC3155079  PMID: 21886616
ACC; dopamine; reward; reinforcement learning; conflict monitoring; volatility; error likelihood
11.  Depression, rumination and the default network 
Major depressive disorder (MDD) has been characterized by excessive default-network activation and connectivity with the subgenual cingulate. These hyper-connectivities are often interpreted as reflecting rumination, where MDDs perseverate on negative, self-referential thoughts. However, the relationship between connectivity and rumination has not been established. Furthermore, previous research has not examined how connectivity with the subgenual cingulate differs when individuals are engaged in a task or not. The purpose of the present study was to examine connectivity of the default network specifically in the subgenual cingulate both on- and off-task, and to examine the relationship between connectivity and rumination. Analyses using a seed-based connectivity approach revealed that MDDs show more neural functional connectivity between the posterior-cingulate cortex and the subgenual-cingulate cortex than healthy individuals during rest periods, but not during task engagement. Importantly, these rest-period connectivities correlated with behavioral measures of rumination and brooding, but not reflection.
doi:10.1093/scan/nsq080
PMCID: PMC3190207  PMID: 20855296
depression; rumination; default network; subgenual cingulate; functional magnetic resonance imaging
12.  Grooming Coercion and the Post-Conflict Trading of Social Services in Wild Barbary Macaques 
PLoS ONE  2011;6(10):e26893.
In animal and human societies, social services such as protection from predators are often exchanged between group members. The tactics that individuals display to obtain a service depend on its value and on differences between individuals in their capacity to aggressively obtain it. Here we analysed the exchange of valuable social services (i.e. grooming and relationship repair) in the aftermath of a conflict, in wild Barbary macaques (Macaca sylvanus). The relationship repair function of post-conflict affiliation (i.e. reconciliation) was apparent in the victim but not in the aggressor. Conversely, we found evidence for grooming coercion by the aggressor; when the victim failed to give grooming soon after a conflict they received renewed aggression from the aggressor. We argue that post-conflict affiliation between former opponents can be better described as a trading of social services rather than coercion alone, as both animals obtain some benefits (i.e. grooming for the aggressor and relationship repair for the victim). Our study is the first to test the importance of social coercion in the aftermath of a conflict. Differences in competitive abilities can affect the exchange of services and the occurrence of social coercion in animal societies. This may also help explain the variance between populations and species in their social behaviour and conflict management strategies.
doi:10.1371/journal.pone.0026893
PMCID: PMC3202593  PMID: 22046398
13.  Bayesian Prediction and Evaluation in the Anterior Cingulate Cortex 
The dorsal anterior cingulate cortex (dACC) has been implicated in a variety of cognitive control functions, among them the monitoring of conflict, error, and volatility, error anticipation, reward learning, and reward prediction errors. In this work, we used a Bayesian ideal observer model, which predicts trial-by-trial probabilistic expectation of stop trials and response errors in the stop signal task, to differentiate these proposed functions quantitatively. We found that dACC hemodynamic response, as measured by functional magnetic resonance imaging, encodes both the absolute prediction error between stimulus expectation and outcome, and the signed prediction error related to response outcome. After accounting for these factors, dACC has no residual correlation with conflict or error likelihood in the stop-signal task. Consistent with recent monkey neural recording studies, and in contrast with other neuroimaging studies, our work demonstrates that dACC reports at least two different types of prediction errors, and beyond contexts that are limited to reward processing.
doi:10.1523/JNEUROSCI.2201-12.2013
PMCID: PMC3711643  PMID: 23365241
cognitive control; Bayesian surprise; prediction error; fMRI; ACC
14.  An fMRI investigation of racial paralysis 
We explore the existence and underlying neural mechanism of a new norm endorsed by both black and white Americans for managing interracial interactions: “racial paralysis’, the tendency to opt out of decisions involving members of different races. We show that people are more willing to make choices—such as who is more intelligent, or who is more polite—between two white individuals (same-race decisions) than between a white and a black individual (cross-race decisions), a tendency which was evident more when judgments involved traits related to black stereotypes. We use functional magnetic resonance imaging to examine the mechanisms underlying racial paralysis, to examine the mechanisms underlying racial paralysis, revealing greater recruitment of brain regions implicated in socially appropriate behavior (ventromedial prefrontal cortex), conflict detection (anterior cingulate cortex), deliberative processing (dorsolateral prefrontal cortex), and inhibition (ventrolateral prefrontal cortex). We also discuss the impact of racial paralysis on the quality of interracial relations.
doi:10.1093/scan/nss010
PMCID: PMC3624949  PMID: 22267521
race; prejudice; inhibition; choice
15.  Volumetric Correlates of Spatiotemporal Working and Recognition Memory Impairment in Aged Rhesus Monkeys 
Cerebral Cortex (New York, NY)  2010;21(7):1559-1573.
Spatiotemporal and recognition memory are affected by aging in humans and macaque monkeys. To investigate whether these deficits are coupled with atrophy of memory-related brain regions, T1-weighted magnetic resonance images were acquired and volumes of the cerebrum, ventricles, prefrontal cortex (PFC), calcarine cortex, hippocampus, and striatum were quantified in young and aged rhesus monkeys. Subjects were tested on a spatiotemporal memory procedure (delayed response [DR]) that requires the integrity of the PFC and a medial temporal lobe-dependent recognition memory task (delayed nonmatching to sample [DNMS]). Region of interest analyses revealed that age inversely correlated with striatal, dorsolateral prefrontal cortex (dlPFC), and anterior cingulate cortex volumes. Hippocampal volume predicted acquisition of the DR task. Striatal volume correlated with DNMS acquisition, whereas total prefrontal gray matter, prefrontal white matter, and dlPFC volumes each predicted DNMS accuracy. A regional covariance analysis revealed that age-related volumetric changes could be captured in a distributed network that was coupled with declining performance across delays on the DNMS task. This volumetric analysis adds to growing evidence that cognitive aging in primates arises from region-specific morphometric alterations distributed across multiple memory-related brain systems, including subdivisions of the PFC.
doi:10.1093/cercor/bhq210
PMCID: PMC3116736  PMID: 21127015
age-related memory impairment; medial temporal lobe; MRI; prefrontal cortex; rhesus monkey
16.  Event-related potentials elicited by errors during the stop-signal task. I: Macaque monkeys 
The error-related negativity (ERN) and positivity (Pe) are components of event-related potential (ERP) waveforms recorded from humans that are thought to reflect performance monitoring. Error-related signals have also been found in single-neuron responses and local-field potentials recorded in supplementary eye field and anterior cingulate cortex of macaque monkeys. However, the homology of these neural signals across species remains controversial. Here, we show that monkeys exhibit ERN and Pe components when they commit errors during a saccadic stop-signal task. The voltage distributions and current densities of these components were similar to those found in humans performing the same task. Subsequent analyses show that neither stimulus- nor response-related artifacts accounted for the error-ERPs. This demonstration of macaque homologues of the ERN and Pe forms a keystone in the bridge linking human and nonhuman primate studies on the neural basis of performance monitoring.
doi:10.1523/JNEUROSCI.3349-11.2011
PMCID: PMC3241968  PMID: 22049407
17.  Medial prefrontal cortex as an action-outcome predictor 
Nature neuroscience  2011;14(10):1338-1344.
The medial prefrontal cortex (mPFC) and especially anterior cingulate cortex (ACC) is central to higher cognitive function and numerous clinical disorders, yet its basic function remains in dispute. Various competing theories of mPFC have treated effects of errors, conflict, error likelihood, volatility, and reward, based on findings from neuroimaging and neurophysiology in humans and monkeys. To date, no single theory has been able to reconcile and account for the variety of findings. Here we show that a simple model based on standard learning rules can simulate and unify an unprecedented range of known effects in mPFC. The model reinterprets many known effects and suggests a new view of mPFC, as a region concerned with learning and predicting the likely outcomes of actions, whether good or bad. Cognitive control at the neural level is then seen as a result of evaluating the probable and actual outcomes of one's actions.
doi:10.1038/nn.2921
PMCID: PMC3183374  PMID: 21926982
18.  Influence of anti-Nogo-A antibody treatment on the reorganization of callosal connectivity of the premotor cortical areas following unilateral lesion of primary motor cortex (M1) in adult macaque monkeys 
Following unilateral lesion of the primary motor cortex, the reorganization of callosal projections from the intact hemisphere to the ipsilesional premotor cortex (PM) was investigated in 7 adult macaque monkeys, in absence of treatment (control; n = 4) or treated with function blocking antibodies against the neurite growth inhibitory protein Nogo-A (n = 3). After functional recovery, though incomplete, the tracer biotinylated dextran amine (BDA) was injected in the ipsilesional PM. Retrogradely labelled neurons were plotted in the intact hemisphere and their number was normalized with respect to the volume of the core of BDA injection sites. (1) The callosal projections to PM in the controls originate mainly from homotypic PM areas and, but to a somewhat lesser extent, from the mesial cortex (cingulate and supplementary motor areas). (2) In the lesioned anti-Nogo-A antibody-treated monkeys, the normalized number of callosal retrogradely labelled neurons was up to several folds higher than in controls, especially in the homotypic PM areas. (3) Except one control with a small lesion and a limited, transient deficit, the anti-Nogo-A antibody-treated monkeys recovered to nearly baseline levels of performance (73–90 %), in contrast to persistent deficits in the control monkeys. These results are consistent with a sprouting and/or sparing of callosal axons promoted by the anti-Nogo-A antibody treatment after lesion of the primary motor cortex, as compared to untreated monkeys.
doi:10.1007/s00221-012-3262-x
PMCID: PMC3483106  PMID: 22990293
Reorganization; Callosal connectivity; Lesion; Tract-tracing
19.  A rate code for sound azimuth in monkey auditory cortex: implications for human neuroimaging studies 
Is sound location represented in the auditory cortex of humans and monkeys? Human neuroimaging experiments have had only mixed success at demonstrating sound location sensitivity in primary auditory cortex. This is in apparent conflict with studies in monkeys and other animals, where single-unit recording studies have found stronger evidence for spatial sensitivity. Does this apparent discrepancy reflect a difference between humans and animals, or does it reflect differences in the sensitivity of the methods used for assessing the representation of sound location? The sensitivity of imaging methods such as fMRI depends on two key aspects of the underlying neuronal population: (1) what kind of spatial sensitivity individual neurons exhibit, and (2) whether neurons with similar response preferences are clustered within the brain.
To address this question, we conducted a single unit recording study in monkeys. We investigated the nature of spatial sensitivity in individual auditory cortical neurons to determine whether they have receptive fields (place code) or monotonic (rate code) sensitivity to sound azimuth. Secondly, we tested how strongly the population of neurons favors contralateral locations. We report here that the majority of neurons show predominantly monotonic azimuthal sensitivity, forming a rate code for sound azimuth, but that at the population level the degree of contralaterality is modest. This suggests that the weakness of the evidence for spatial sensitivity in human neuroimaging studies of auditory cortex may be due to limited lateralization at the population level, despite what may be considerable spatial sensitivity in individual neurons.
doi:10.1523/JNEUROSCI.5044-07.2008
PMCID: PMC3654685  PMID: 18385333
sound location; rate code; place code; neuroimaging; auditory cortex; Primate
20.  Resting State Functional Connectivity within the Cingulate Cortex Jointly Predicts Agreeableness and Stressor-Evoked Cardiovascular Reactivity 
NeuroImage  2010;55(1):363-370.
Exaggerated cardiovascular reactivity to stress confers risk for cardiovascular disease. Further, individual differences in stressor-evoked cardiovascular reactivity covary with the functionality of cortical and limbic brain areas, particularly within the cingulate cortex. What remains unclear, however, is how individual differences in personality traits interact with cingulate functionality in the prediction of stressor-evoked cardiovascular reactivity. Accordingly, we tested the associations between (i) a particular personality trait, Agreeableness, which is associated with emotional reactions to conflict, (ii) resting state functional connectivity within the cingulate cortex, and (iii) stressor-evoked blood pressure (BP) reactivity. Participants (N=39, 19 men, aged 20–37 yrs) completed a resting functional connectivity MRI protocol, followed by two standardized stressor tasks that engaged conflict processing and evoked BP reactivity. Agreeableness covaried positively with BP reactivity across individuals. Moreover, connectivity analyses demonstrated that a more positive functional connectivity between the posterior cingulate (BA31) and the perigenual anterior cingulate (BA32) covaried positively with Agreeableness and with BP reactivity. Finally, statistical mediation analyses demonstrated that BA31–BA32 connectivity mediated the covariation between Agreeableness and BP reactivity. Functional connectivity within the cingulate appears to link Agreeableness and a risk factor for cardiovascular disease, stressor-evoked BP reactivity.
doi:10.1016/j.neuroimage.2010.11.064
PMCID: PMC3031759  PMID: 21130172
agreeableness; cingulate; personality; resting state connectivity; stressor-evoked cardiovascular reactivity
21.  Short-term effects of unilateral lesion of the primary motor cortex (M1) on ipsilesional hand dexterity in adult macaque monkeys 
Brain Structure & Function  2011;217(1):63-79.
Although the arrangement of the corticospinal projection in primates is consistent with a more prominent role of the ipsilateral motor cortex on proximal muscles, rather than on distal muscles involved in manual dexterity, the role played by the primary motor cortex on the control of manual dexterity for the ipsilateral hand remains a matter a debate, either in the normal function or after a lesion. We, therefore, tested the impact of permanent unilateral motor cortex lesion on the manual dexterity of the ipsilateral hand in 11 macaque monkeys, within a time window of 60 days post-lesion. For comparison, unilateral reversible pharmacological inactivation of the motor cortex was produced in an additional monkey. Manual dexterity was assessed quantitatively based on three motor parameters derived from two reach and grasp manual tasks. In contrast to the expected dramatic, complete deficit of manual dexterity of the contralesional hand that persists for several weeks, the impact on the manual dexterity of the ipsilesional hand was generally moderate (but statistically significant) and, when present, lasted less than 20 days. Out of the 11 monkeys, only 3 showed a deficit of the ipsilesional hand for 2 of the 3 motor parameters, and 4 animals had a deficit for only one motor parameter. Four monkeys did not show any deficit. The reversible inactivation experiment yielded results consistent with the permanent lesion data. In conclusion, the primary motor cortex exerts a modest role on ipsilateral manual dexterity, most likely in the form of indirect hand postural control.
doi:10.1007/s00429-011-0327-8
PMCID: PMC3249543  PMID: 21597965
Permanent lesion; Reversible lesion; Primate
22.  UNDERSTANDING THE PARIETAL LOBE SYNDROME FROM A NEUROPHYSIOLOGICAL AND EVOLUTIONARY PERSPECTIVE 
The European journal of neuroscience  2010;31(12):2320-2340.
In human and non-human primates parietal cortex is formed by a multiplicity of areas. For those of the Superior Parietal Lobule (SPL) there exists a certain homology between man and macaques. As a consequence, Optic Ataxia, a disturbed visual control of hand reaching, has similar features in man and monkeys. Establishing such correspondence has proven difficult for the areas of the Inferior Parietal Lobule (IPL). This difficulty depends on many factors. First, no physiological information is available in man on the dynamic properties of cells in the IPL. Second, the number of IPL areas identified in the monkey is paradoxically higher that that so far described in man, although this issue will probably be reconsidered in future years, thanks to comparative imaging studies. Third, the consequences of parietal lesions in monkeys do not always match those observed in humans. This is another paradox if one considers that, in certain cases, the functional properties of neurons in the monkeys IPL would predict the presence of behavioral skills, such as construction capacity, that however do not seem to emerge in the wild. Therefore, Constructional Apraxia, which is well characterized in man, has never been described in monkeys and apes. Finally, only certain aspects, i.e. hand Directional Hypokinesia and Gaze Apraxia (Balint's Psychic Paralysis of Gaze), of the multifaceted syndrome Hemispatial Neglect have been described in monkeys. These similarities, differences and paradoxes, among many others, make the study of the evolution and function of parietal cortex a challenging “case”.
doi:10.1111/j.1460-9568.2010.07291.x
PMCID: PMC2900452  PMID: 20550568
parietal syndrome; behavioral neurophysiology; neuroanatomy; neuropsychology; evolution
23.  A computational model of risk, conflict, and individual difference effects in the anterior cingulate cortex 
Brain research  2007;1202:99-108.
The error likelihood effect in anterior cingulate cortex (ACC) has recently been shown to be a special case of an even more general risk prediction effect, which signals both the likelihood of an error and the potential severity of its consequences. Surprisingly, these error likelihood and anticipated consequence effects are strikingly absent in risk-taking individuals. Conversely, conflict effects in ACC were found to be stronger in these same individuals. Here we show that the error likelihood computational model can account for individual differences in error likelihood, predicted error consequence, and conflict effects in ACC with no changes from the published version of the model. In particular, the model accounts for the counter-intuitive inverse relationship between conflict and error likelihood effects as a function of the ACC learning rate in response to errors. As the learning rate increases, ACC learns more effectively from mistakes, which increases risk prediction effects at the expense of conflict effects. Thus, the model predicts that individuals with faster error-based learning in ACC will be more risk averse and show greater ACC error likelihood effects but smaller ACC conflict effects. Furthermore, the model suggests that apparent response conflict effects in ACC may actually consist of two related effects: increased error likelihood and a greater number of simultaneously cued responses, whether or not the responses are mutually incompatible. The results clarify the basic computational mechanisms of learned risk aversion and may have broad implications for predicting and managing risky behavior in healthy and clinical populations.
doi:10.1016/j.brainres.2007.06.080
PMCID: PMC2322871  PMID: 17707352
anterior cingulate; conflict; individual differences; computational model; dopamine
24.  Distinct Encoding of Spatial and Nonspatial Visual Information in Parietal Cortex 
It is well established that the primate parietal cortex plays an important role in visuospatial processing. Parietal cortex damage in both humans and monkeys can lead to behavioral deficits in spatial processing, and many parietal neurons, such as in the macaque lateral intraparietal area (LIP), are strongly influenced by visual–spatial factors. Several recent studies have shown that LIP neurons can also convey robust signals related to nonspatial factors, such as color, shape, and the behavioral context or rule that is relevant for solving the task at hand. But what is the relationship between the encoding of spatial factors and more abstract, nonspatial, influences in LIP? To examine this, we trained monkeys to group visual motion patterns into two arbitrary categories, and recorded the activity of LIP neurons while monkeys performed a categorization task in which stimuli were presented either inside each neuron's receptive field (RF) or at a location in the opposite visual field. While the activity of nearly all LIP neurons showed strong spatial dependence (i.e., greater responses when stimuli were presented within neurons’ RFs), we also found that many LIP neurons also showed reliable encoding of the category membership of stimuli even when the stimuli were presented away from neurons’ RFs. This suggests that both spatial and nonspatial information can be encoded by individual LIP neurons, and that parietal cortex may be a nexus for the integration of visuospatial signals and more abstract task-dependent information during complex visually based behaviors.
doi:10.1523/JNEUROSCI.2878-08.2009
PMCID: PMC2898938  PMID: 19403833
25.  Distinct Parietal and Temporal Pathways to the Homologues of Broca's Area in the Monkey 
PLoS Biology  2009;7(8):e1000170.
An unprecedented detailed analysis of ventrolateral frontal cortical circuitry in Broca's area of the non-human primate brain clarifies the functional pathways permitting interaction between posterior cortical areas and the anterior language zone, providing important clues about the evolution of language.
The homologues of the two distinct architectonic areas 44 and 45 that constitute the anterior language zone (Broca's region) in the human ventrolateral frontal lobe were recently established in the macaque monkey. Although we know that the inferior parietal lobule and the lateral temporal cortical region project to the ventrolateral frontal cortex, we do not know which of the several cortical areas found in those regions project to the homologues of Broca's region in the macaque monkey and by means of which white matter pathways. We have used the autoradiographic method, which permits the establishment of the cortical area from which axons originate (i.e., the site of injection), the precise course of the axons in the white matter, and their termination within particular cortical areas, to examine the parietal and temporal connections to area 44 and the two subdivisions of area 45 (i.e., areas 45A and 45B). The results demonstrated a ventral temporo-frontal stream of fibers that originate from various auditory, multisensory, and visual association cortical areas in the intermediate superolateral temporal region. These axons course via the extreme capsule and target most strongly area 45 with a more modest termination in area 44. By contrast, a dorsal stream of axons that originate from various cortical areas in the inferior parietal lobule and the adjacent caudal superior temporal sulcus was found to target both areas 44 and 45. These axons course in the superior longitudinal fasciculus, with some axons originating from the ventral inferior parietal lobule and the adjacent superior temporal sulcus arching and forming a simple arcuate fasciculus. The cortex of the most rostral part of the inferior parietal lobule is preferentially linked with the ventral premotor cortex (ventral area 6) that controls the orofacial musculature. The cortex of the intermediate part of the inferior parietal lobule is linked with both areas 44 and 45. These findings demonstrate the posterior parietal and temporal connections of the ventrolateral frontal areas, which, in the left hemisphere of the human brain, were adapted for various aspects of language production. These precursor circuits that are found in the nonlinguistic, nonhuman, primate brain also exist in the human brain. The possible reasons why these areas were adapted for language use in the human brain are discussed. The results throw new light on the prelinguistic precursor circuitry of Broca's region and help understand functional interactions between Broca's ventrolateral frontal region and posterior parietal and temporal association areas.
Author Summary
Two distinct cortical areas in the frontal lobe of the human brain, known as Broca's region, are involved with language production. This region has also been shown to exist in nonhuman primates. In this study, we explored the precise neural connectivity of Broca's region in macaque monkeys using the autoradiographic method to achieve a level of detail impossible in the human brain. We identified two major streams of connections feeding into Broca's area: a ventral stream from the temporal region, which includes areas processing auditory, multisensory, and visual information and a dorsal stream originating from the inferior parietal lobule and the adjacent superior temporal sulcus. Our detailed connectivity analysis illuminates the pathways via which posterior cortical areas can interact functionally with Broca's region, in addition to contributing to an understanding of the evolution of language. We suggest that a fundamental function of Broca's region is to retrieve information in a controlled strategic way from posterior cortical regions and to translate this information into action. This fundamental function was adapted during evolution of the left hemisphere of the human brain to serve language.
doi:10.1371/journal.pbio.1000170
PMCID: PMC2714989  PMID: 19668354

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