Parietal–frontal networks in primate brains are central to mediating actions. Physiological and anatomical investigations have shown that the parietal–frontal network is consistently organized across several branches of primate evolution that include prosimian galagos, New World owl and squirrel monkeys, and Old World macaque monkeys. Electrical stimulation with 0.5-sec trains of pulses delivered via microelectrodes evoked ethologically relevant actions from both posterior parietal cortex (PPC) and frontal motor cortex (FMC). Reaching, grasping, defensive, and other complex movement patterns were evoked from domains that had a characteristic organization in both FMC and PPC. Although a PPC domain (e.g. reaching) may be connected with other PPC domains (e.g. grasping and defensive), its connections with FMC are preferential for a matching domain (reaching). Similarly, electrical stimulation of a PPC domain and concurrent optical imaging of FMC, showed activation patterns consistent with the preferential connectivity of PPC and FMC domains. The evidence for similar arrangements of interconnected functional domains in PPC and FMC of members of three major branches of the primate radiation suggests that the parietal–frontal networks emerged early in the evolution of primates. The small size of PPC in the close relatives of primates including lagomorphs, rodents, and tree shrews, suggests a limited involvement of PPC in motor behavior before archaic primates emerged. However, functional domains may have evolved in motor cortex before the emergence of archaic primates.
motor cortex; posterior parietal cortex; grasping; prosimians
In all primates, the cortical control of hand and arm movements is initiated and controlled by a network of cortical regions including primary motor cortex (M1), premotor cortex (PM), and posterior parietal cortex (PPC). These interconnected regions are influenced by inputs from especially visual and somatosensory cortical areas, and prefrontal cortex. Here we discuss recent evidence showing M1, PM, and PPC can be subdivided into a number of functional zones or domains, including several that participate in guiding and controlling hand and arm movements. Functional zones can be defined by the movement sequences evoked by microstimulation within them, and functional zones related to the same type of movement in all three cortical regions are interconnected. The inactivation of a functional zone in each of the regions has a different impact on motor behavior. Finally, there is considerable plasticity within the networks so that behavioral recoveries can occur after damage to functional zones within a network.
The superior colliculus (SC) is a key structure within the extrageniculate pathway of visual information to cortex and is highly involved in visuomotor functions. Previous studies in anthropoid primates have shown that superficial layers of the SC receive direct inputs from various visual cortical areas such as V1, V2, and middle temporal (MT), while deeper layers receive direct inputs from visuomotor cortical areas within the posterior parietal cortex and the frontal eye fields. Very little is known, however, about the corticotectal projections in prosimian primates. In the current study we investigated the sources of cortical inputs to the SC in prosimian galagos (Otolemur garnetti) using retrograde anatomical tracers placed into the SC. The superficial layers of the SC in galagos received the majority of their inputs from early visual areas and visual areas within the MT complex. Yet, surprisingly, MT itself had relatively few corticotectal projections. Deeper layers of the SC received direct projections from visuomotor areas including the posterior parietal cortex and premotor cortex. However, relatively few corticotectal projections originated within the frontal eye fields. While prosimian galagos resemble other primates in having early visual areas project to the superficial layers of the SC, with higher visuomotor regions projecting to deeper layers, the results suggest that MT and frontal eye field projections to the SC were sparse in early primates, remained sparse in present-day prosimian primates, and became more pronounced in anthropoid primates.
visual cortex; FEF; LIP; MT; primates
We can learn about the evolution of neocortex in primates through comparative studies of cortical organization in primates and those mammals that are the closest living relatives of primates, in conjunction with brain features revealed by the skull endocasts of fossil archaic primates. Such studies suggest that early primates had acquired a number of features of neocortex that now distinguish modern primates. Most notably, early primates had an array of new visual areas, and those visual areas widely shared with other mammals had been modified. Posterior parietal cortex was greatly expanded with sensorimotor modules for reaching, grasping, and personal defense. Motor cortex had become more specialized for hand use, and the functions of primary motor cortex were enhanced by the addition and development of premotor and cingulate motor areas. Cortical architecture became more varied, and cortical neuron populations became denser overall than in nonprimate ancestors. Primary visual cortex had the densest population of neurons, and this became more pronounced in the anthropoid radiation. Within the primate clade, considerable variability in cortical size, numbers of areas, and architecture evolved.
prosimians; tarsiers; anthropoids; sensory cortex; motor cortex
Short-tailed opossums (Monodelphis domestica) belong to the branch of marsupial mammals that diverged from eutherian mammals approximately 180 million years ago. They are small in size, lack a marsupial pouch, and may have retained more morphological characteristics of early marsupial neocortex than most other marsupials. In the present study, we used several different histochemical and immunochemical procedures to reveal the architectonic characteristics of cortical areas in short-tailed opossums. Subdivisions of cortex were identified in brain sections cut in the coronal, sagittal, horizontal or tangential planes and processed for a calcium-binding protein, parvalbumin (PV), neurofilament protein epitopes recognized by SMI-32, the vesicle glutamate transporter 2 (VGluT2), myelin, cytochrome oxidase (CO), and Nissl substance. These different procedures revealed similar boundaries among areas, suggesting that functionally relevant borders were detected. The results allowed a fuller description and more precise demarcation of previously identified sensory areas, and the delineation of additional subdivisions of cortex. Area 17 (V1) was especially prominent, with a densely populated layer 4, high myelination levels, and dark staining of PV and VGluT2 immunopositive terminations. These architectonic features were present, albeit less pronounced, in somatosensory and auditory cortex. The major findings support the conclusion that short-tailed opossums have fewer cortical areas and their neocortex is less distinctly laminated than most other mammals.
Marsupial; Cortical areas; Visual cortex; Frontal cortex; Somatosensory cortex; Auditory cortex; Retrosplenial cortex; Cingulate cortex
The pulvinar complex of prosimian primates is not as architectonically differentiated as that of anthropoid primates. Thus, the functional subdivisions of the complex have been more difficult to determine. In the present study, we related patterns of connections of cortical visual areas (primary visual area, V1; secondary visual area, V2; and middle temporal visual area, MT) as well as the superior colliculus of the visual midbrain, with subdivisions of the pulvinar complex of prosimian galagos (Otolemur garnetti) that were revealed in brain sections processed for cell bodies (Nissl), cytochrome oxidase, or myelin. As in other primates, the architectonic methods allowed us to distinguish the lateral pulvinar (PL) and inferior pulvinar (PI) as major divisions of the visual pulvinar. The connection patterns further allowed us to divide PI into a large central nucleus (PIc), a medial nucleus (PIm), and a posterior nucleus (PIp). Both PL and PIc have separate topographic patterns of connections with V1 and V2. A third, posterior division of PI, PIp, does not appear to project to V1 and V2 and is further distinguished by receiving inputs from the superior colliculus. All these subdivisions of PI project to MT. The evidence suggests that PL of galagos contains a single, large nucleus, as in monkeys, and that PI may have only three subdivisions, rather than the four subdivisions of monkeys. In addition, the cortical projections of PI nuclei are more widespread than those in monkeys. Thus, the pulvinar nuclei in prosimian primates and anthropoid primates have evolved along somewhat different paths.
superior colliculus; visual cortex; middle temporal area; area 17; area 18; primate evolution; thalamus
The architectonic features of the ventroposterior nucleus (VP) were visualized in coronal brain sections from two macaque monkeys, two owl monkeys, two squirrel monkeys, and three galagos that were processed for cytochrome oxidase, Nissl bodies, or the vesicular glutamate transporter 2 (vGluT2). The traditional ventroposterior medial (VPM) and ventroposterior lateral (VPL) subnuclei were easily identified, as well as the forelimb and hindlimb compartments of VPL, as they were separated by poorly staining, cell-poor septa. Septa also separated other cell groups within VPM and VPL, specifically in the medial compartment of VPL representing the hand (hand VPL). In one squirrel monkey and one galago we demonstrated that these five groups of cells represent digits 1–5 in a mediolateral sequence by injecting tracers into the cortical representation of single digits, defined by microelectrode recordings, and relating concentrations of labeled neurons to specific cell groups in hand VPL. The results establish the existence of septa that isolate the representation of the five digits in VPL of primates and demonstrate that the isolated cell groups represent digits 1–5 in a mediolateral sequence. The present results show that the septa are especially prominent in brain sections processed for vGluT2, which is expressed in the synaptic terminals of excitatory neurons in most nuclei of the brainstem and thalamus. As vGluT2 is expressed in the synaptic terminations from dorsal columns and trigeminal brainstem nuclei, the effectiveness of vGluT2 preparations in revealing septa in VP likely reflects a lack of synapses using glutamate in the septa. J. Comp. Neurol. 519:738–758, 2011.
area 3b; somatosensory maps; digit representation; vGluT2
Connections of primary (V1) and secondary (V2) visual areas were revealed in macaque monkeys ranging in age from 2 to 16 weeks by injecting small amounts of cholera toxin subunit B (CTB). Cortex was flattened and cut parallel to the surface to reveal injection sites, patterns of labeled cells, and patterns of cytochrome oxidase (CO) staining. Projections from the lateral geniculate nucleus and pulvinar to V1 were present at 4 weeks of age, as were pulvinar projections to thin and thick CO stripes in V2. Injections into V1 in 4- and 8-week-old monkeys labeled neurons in V2, V3, middle temporal area (MT), and dorsolateral area (DL)/V4. Within V1 and V2, labeled neurons were densely distributed around the injection sites, but formed patches at distances away from injection sites. Injections into V2 labeled neurons in V1, V3, DL/V4, and MT of monkeys 2-, 4-, and 8-weeks of age. Injections in thin stripes of V2 preferentially labeled neurons in other V2 thin stripes and neurons in the CO blob regions of V1. A likely thick stripe injection in V2 at 4 weeks of age labeled neurons around blobs. Most labeled neurons in V1 were in superficial cortical layers after V2 injections, and in deep layers of other areas. Although these features of adult V1 and V2 connectivity were in place as early as 2 postnatal weeks, labeled cells in V1 and V2 became more restricted to preferred CO compartments after 2 weeks of age.
V1; V2; pulvinar; lateral geniculate nucleus; macaque monkey
Cell and neuron densities vary across the cortical sheet in a predictable manner across different primate species (Collins et al., 2010b). Primary motor cortex, M1, is characterized by lower neuron densities relative to other cortical areas. M1 contains a motor representation map of contralateral body parts from tail to tongue in a mediolateral sequence. Different functional movement representations within M1 likely require specialized microcircuitry for control of different body parts, and these differences in circuitry may be reflected by variation in cell and neuron densities. Here we determined cell and neuron densities for multiple sub-regions of M1 in six primate species, using the semi-automated flow fractionator method. The results verify previous reports of lower overall neuron densities in M1 compared to other parts of cortex in the six primate species examined. The most lateral regions of M1 that correspond to face and hand movement representations, are more neuron dense relative to medial locations in M1, which suggests differences in cortical circuitry within movement zones.
M1; flow fractionator; isotropic fractionator; movement
Inferences about how the complex sensory and motor systems of the human brain evolved are based on the results of comparative studies of brain organization across a range of mammalian species, and evidence from the endocasts of fossil skulls of key extinct species. The endocasts of the skulls of early mammals indicate that they had small brains with little neocortex. Evidence from comparative studies of cortical organization from small-brained mammals of the six major branches of mammalian evolution supports the conclusion that the small neocortex of early mammals was divided into roughly 20–25 cortical areas, including primary and secondary sensory fields. In early primates, vision was the dominant sense, and cortical areas associated with vision in temporal and occipital cortex underwent a significant expansion. Comparative studies indicate that early primates had 10 or more visual areas, and somatosensory areas with expanded representations of the forepaw. Posterior parietal cortex was also expanded, with a caudal half dominated by visual inputs, and a rostral half dominated by somatosensory inputs with outputs to an array of seven or more motor and visuomotor areas of the frontal lobe. Somatosensory areas and posterior parietal cortex became further differentiated in early anthropoid primates. As larger brains evolved in early apes and in our hominin ancestors, the number of cortical areas increased to reach an estimated 200 or so in present day humans, and hemispheric specializations emerged. The large human brain grew primarily by increasing neuron number rather than increasing average neuron size.
The visual pulvinar is part of the dorsal thalamus, and in primates it is especially well developed. Recently, our understanding of how the visual pulvinar is subdivided into nuclei has greatly improved as a number of histological procedures have revealed marked architectonic differences within the pulvinar complex. At the same time, there have been unparalleled advances in understanding of how visual cortex of primates is subdivided into areas and how these areas interconnect. In addition, considerable evidence supports the view that the hierarchy of interconnected visual areas is divided into two major processing streams, a ventral stream for object vision, and a dorsal stream for visually guided actions. In this review, we present evidence that a subset of medial nuclei in the inferior pulvinar function predominantly as a subcortical component of the dorsal stream while the most lateral nucleus of the inferior pulvinar and the adjoining ventrolateral nucleus of the lateral pulvinar are more devoted to the ventral stream of cortical processing. These nuclei provide cortico-pulvinar-cortical interactions that spread information across areas within streams, as well as information relayed from the superior colliculus via inferior pulvinar nuclei to largely dorsal stream areas.
visual system; superior colliculus; visual cortex; thalamus
After 100 years of progress in understanding the organization of cerebral cortex, three issues have persisted over the last 35 years, which are revisited in this paper. First, is V3 an established or questionable area of visual cortex? Second, does taste cortex include part of area 3b (S1 proper) and other somatosensory areas? Third, is primary auditory cortex, A1, of primates the homologue of A1 in cats? The existence of such questions about even the early stages of cortical processing reflects the difficulties in mapping cerebral cortex, and reminds us that the era of basic discovery is far from over.
gustatory cortex; V3; auditory cortex; somatosensory cortex; visual cortex
The structure of the brain as a product of morphogenesis is difficult to reconcile with the observed complexity of cerebral connectivity. We therefore analyzed relationships of adjacency and crossing between cerebral fiber pathways in four nonhuman primate species and in humans by using diffusion magnetic resonance imaging. The cerebral fiber pathways formed a rectilinear three-dimensional grid continuous with the three principal axes of development. Cortico-cortical pathways formed parallel sheets of interwoven paths in the longitudinal and medio-lateral axes, in which major pathways were local condensations. Cross-species homology was strong and showed emergence of complex gyral connectivity by continuous elaboration of this grid structure. This architecture naturally supports functional spatio-temporal coherence, developmental path-finding, and incremental rewiring with correlated adaptation of structure and function in cerebral plasticity and evolution.
In response to Catani et al., we show that corticospinal pathways adhere via sharp turns to two local grid orientations; that our studies have three times the diffusion resolution of those compared; and that the noted technical concerns, including crossing angles, do not challenge the evidence of mathematically specific geometric structure. Thus, the geometric thesis gives the best account of the available evidence.
Relating stimulus properties to the response properties of individual neurons and neuronal networks is a major goal of sensory research. Many investigators implant electrode arrays in multiple brain areas and record from chronically implanted electrodes over time to answer a variety of questions. Technical challenges related to analyzing large-scale neuronal recording data are not trivial. Several analysis methods traditionally used by neurophysiologists do not account for dependencies in the data that are inherent in multi-electrode recordings. In addition, when neurophysiological data are not best modeled by the normal distribution and when the variables of interest may not be linearly related, extensions of the linear modeling techniques are recommended. A variety of methods exist to analyze correlated data, even when data are not normally distributed and the relationships are nonlinear. Here we review expansions of the Generalized Linear Model designed to address these data properties. Such methods are used in other research fields, and the application to large-scale neuronal recording data will enable investigators to determine the variable properties that convincingly contribute to the variances in the observed neuronal measures. Standard measures of neuron properties such as response magnitudes can be analyzed using these methods, and measures of neuronal network activity such as spike timing correlations can be analyzed as well. We have done just that in recordings from 100-electrode arrays implanted in the primary somatosensory cortex of owl monkeys. Here we illustrate how one example method, Generalized Estimating Equations analysis, is a useful method to apply to large-scale neuronal recordings.
ANOVA; Generalized Estimating Equations; Generalized Linear Mixed Models; neuronal ensembles; multi-electrode; parallel recordings; primate
In the present study, galago brains were sectioned in the coronal, sagittal or horizontal planes, and sections were processed with several different histochemical and immunohistochemical procedures to reveal the architectonic characteristics of the various cortical areas. The histochemical methods used included the traditional Nissl, cytochrome oxidase and myelin stains, as well as a zinc stain, which reveals free ionic zinc in the axon terminals of neurons. Immunohistochemical methods include parvalbumin (PV) and calbindin (CB), both calcium-binding proteins, and the vesicle glutamate transporter 2 (VGluT2). These different procedures revealed similar boundaries between areas, which suggests that functionally relevant borders were being detected. These results allowed a more precise demarcation of previously identified areas. As thalamocortical terminations lack free ionic zinc, primary cortical areas were most clearly revealed by the zinc stain, due to the poor zinc staining of layer 4. Area 17 was especially prominent, as the broad layer 4 was nearly free of zinc stain. However, this feature was less pronounced in the primary auditory and somatosensory cortex. As VGluT2 is expressed in thalamocortical terminations, layer 4 of primary sensory areas was darkly stained for VGluT2. Primary motor cortex had reduced VGluT2 staining, and increased zinc-enriched terminations in the poorly developed granular layer 4 compared to the adjacent primary somatosensory area. The middle temporal visual (MT) showed increased PV and VGluT2 staining compared to the surrounding cortical areas. The resulting architectonic maps of cortical areas in galagos can usefully guide future studies of cortical organizations and functions.
primate; cortical areas; visual cortex; motor cortex; somatosensory cortex; auditory cortex; prosimian
We used half-second trains of intracortical microstimulation to study the functional organization of the posterior parietal cortex (PPC) in prosimian galagos. These trains of current pulses evoked meaningful behaviors from the anterior, but not posterior, half of PPC. Stimulation of dorsal PPC caused contralateral forelimb movements, including defensive, hand-to-mouth, and reaching movements. Defensive and hand-to-mouth movement territories overlapped, although hand-to-mouth movements were usually evoked from more rostrolateral sites than defensive movements. Reaching movement sites were typically more caudal than defensive or hand-to-mouth movement sites. Stimulation of the most medial PPC sites evoked complex movements of forelimbs and hindlimbs. Ventral PPC commonly represented defensive face movements. Similar defensive movements, with the addition of widely opening the mouth to expose the teeth, were elicited from a small area in front of the PPC defensive face zone. Sometimes defensive face movements occurred with forelimb movements. Thus, subregions of PPC relate to different ethologically relevant categories of behavior. Most movements were initiated within 33–100 msec after stimulus onset. Face, eye blink, and ear movements were generally less delayed than forelimb movements. The present results in galagos, together with those obtained from macaque monkeys by Graziano and coworkers, suggest that the functional involvement of the PPC in specific types of sensorimotor behavior evolved early in the course of primate evolution and that networks for complex movements involving motor and posterior parietal areas are characteristic of all primate brains.
long train stimulation; nonhuman primate; motor behavior; motor cortex
We studied cortical connections of functionally distinct movement zones of the posterior parietal cortex (PPC) in galagos identified by intracortical microstimulation with long stimulus trains (~500 msec). All these zones were in the anterior half of PPC, and each of them had a different pattern of connections with premotor (PM) and motor (M1) areas of the frontal lobe and with other areas of parietal and occipital cortex. The most rostral PPC zone has major connections with motor and visuomotor areas of frontal cortex as well as with somatosensory areas 3a and 1-2 and higher order somatosensory areas in the lateral sulcus. The dorsal part of anterior PPC region representing hand-to-mouth movements is connected mostly to the forelimb representation in PM, M1, 3a, 1-2, and somatosensory areas in the lateral sulcus and on the medial wall. The more posterior defensive and reaching zones have additional connections with nonprimary visual areas (V2, V3, DL, DM, MST). Ventral aggressive and defensive face zones have reciprocal connections with each other as well as connections with mostly face, but also forelimb representations of premotor areas and M1 as well as prefrontal cortex, FEF, and somatosensory areas in the lateral sulcus and areas on the medial surface of the hemisphere. Whereas the defensive face zone is additionally connected to nonprimary visual cortical areas, the aggressive face zone is not. These differences in connections are consistent with our functional parcellation of PPC based on intracortical long-train microstimulation, and they identify parts of cortical networks that mediate different motor behaviors.
intraparietal cortex; motor areas; somatosensory cortex; visual cortex; movement; behavior
As diurnal rodents with a well-developed visual system, squirrels provide a useful comparison of visual system organization with other highly visual mammals such as tree shrews and primates. Here, we describe the projection pattern of gray squirrel superior colliculus (SC) with the large and well-differentiated pulvinar complex. Our anatomical results support the conclusion that the pulvinar complex of squirrels consists of four distinct nuclei. The caudal (C) nucleus, distinct in cytochrome oxidase (CO), acetylcholinesterase (AChE), and vesicular glutamate transporter-2 (VGluT2) preparations, received widespread projections from the ipsilateral SC, although a crude retinotopic organization was suggested. The caudal nucleus also received weaker projections from the contralateral SC. The caudal nucleus also projects back to the ipsilateral SC. Lateral (RLl) and medial (RLm) parts of the previously defined rostral lateral pulvinar (RL) were architectonically distinct, and each nucleus received its own retinotopic pattern of focused ipsilateral SC projections. The SC did not project to the rostral medial (RM) nucleus of the pulvinar. SC injections also revealed ipsilateral connections with the dorsal and ventral lateral geniculate nuclei, nuclei of the pretectum, and nucleus of the brachium of the inferior colliculus and bilateral connections with the parabigeminal nuclei. Comparisons with other rodents suggest that a variously named caudal nucleus, which relays visual inputs from the SC to temporal visual cortex, is common to all rodents and possibly most mammals. RM and RL divisions of the pulvinar complex also appear to have homologues in other rodents.
superior colliculus; pulvinar; dorsal thalamus; lateral geniculate nucleus; rodents
Squirrels are highly visual mammals with an expanded cortical visual system and a number of well-differentiated architectonic fields. In order to describe and delimit cortical fields, subdivisions of cortex were reconstructed from serial brain sections cut in the coronal, sagittal, or horizontal planes. Architectonic characteristics of cortical areas were visualized after brain sections were processed with immunohistochemical and histochemical procedures for revealing parvalbumin, calbindin, neurofilament protein, vesicle glutamate transporter 2, limbic-associated membrane protein, synaptic zinc, cytochrome oxidase, myelin or Nissl substance. In general, these different procedures revealed similar boundaries between areas, suggesting that functionally relevant borders were being detected. The results allowed a more precise demarcation of previously identified areas as well as the identification of areas that had not been previously described. Primary sensory cortical areas characterized by sparse zinc staining of layer 4, as thalamocortical terminations lack zinc, as well as by layer 4 terminations rich in parvalbumin and vesicle glutamate transporter 2. Primary areas also expressed higher levels of cytochrome oxidase and myelin. Primary motor cortex was associated with large SMI-32 labeled pyramidal cells in layers 3 and 5. Our proposed organization of cortex in grey squirrels includes both similarities and differences to the proposed of cortex in other rodents such as mice and rats. The presence of a number of well-differentiated cortical areas in squirrels may serve as a guide to the identification of homologous fields in other rodents, as well as a useful guide in further studies of cortical organization and function.
Rodents; cortical areas; visual cortex; motor cortex; somatosensory cortex; auditory cortex; cingulate cortex; retrosplenial cortex
Tree shrews are small mammals that bear some semblance to squirrels, but are actually close relatives of primates. Thus, they have been extensively studied as a model for the early stages of primate evolution. In the present study, subdivisions of cortex were reconstructed from brain sections cut in the coronal, sagittal or horizontal planes, and processed for parvalbumin (PV), SMI-32 immunopositive neurofilament protein epitopes, vesicle glutamate transporter 2 (VGluT2), free ionic zinc, myelin, cytochrome oxidase (CO) and Nissl substance. These different procedures revealed similar boundaries between areas, suggesting the detection of functionally relevant borders and allowed a more precise demarcation of cortical areal boundaries. Primary cortical areas were most clearly revealed by the zinc stain, due to the poor staining of layer 4, as thalamocortical terminations lack free ionic zinc. Area 17 (V1) was especially prominent, as the broad layer 4 was nearly free of zinc stain. However, this feature was less pronounced in primary auditory and somatosensory, cortex. In primary sensory areas, thalamocortical terminations in layer 4 densely express VGluT2. Auditory cortex consists of two architectonically distinct subdivisions, a primary core region (Ac), surrounded by a belt region (Ab) that had a slightly less developed koniocellular appearance. Primary motor cortex (M1) was identified by the absence of VGluT2 staining in the poorly developed granular layer 4 and the presence of SMI-32 labeled pyramidal cells in layers 3 and 5. The presence of well-differentiated cortical areas in tree shrews indicates their usefulness in studies of cortical organization and function.
Rodents; primates; cortical areas; visual cortex; motor cortex; somatosensory cortex; auditory cortex; cingulate cortex; retrosplenial cortex; insular cortex
The temporal cortex of grey squirrels contains three architectonically distinct regions. One of these regions, the temporal anterior (Ta) region has been identified in previous physiological and anatomical studies as containing several areas that are largely auditory in function. Consistent with this evidence, Ta has architectonic features that are internally somewhat variable, but overall sensory in nature. In contrast, the caudally adjoining temporal intermediate region (Ti) has architectonic features that suggest higher order and possibly multisensory processing. Finally, the most caudal region, composed of previously defined temporal medial (Tm) and temporal posterior (Tp) fields, again has more of the appearance of sensory cortex. To better understand their functional roles, we injected anatomical tracers into these regions to reveal their thalamic connections. As expected, the dorsal portion of Ta, containing two primary or primary-like auditory areas, received inputs from the ventral and magnocellular divisions of the auditory medial geniculate complex, MGv and MGm. The most caudal region, Tm plus Tp, received inputs from the large visual pulvinar of squirrels, possibly accounting for the sensory architectonic characteristics of this region. However, Tp additionally receives inputs from the magnocellular (MGm) and dorsal (MGd) divisions of the medial geniculate complex, implicating Tp in bisensory processing. Finally, the middle region, Ti, had auditory inputs from MGd and MGm, but not from the visual pulvinar, providing evidence that Ti has higher-order auditory functions. The results indicate that the architectonically distinct regions of temporal cortex of squirrels are also functionally distinct. Understanding how temporal cortex is functionally organized in squirrels can guide interpretations of temporal cortex organization in other rodents where architectonic subdivisions are not as obvious.
visual cortex; auditory cortex; multisensory cortex; lateral geniculate nucleus; pulvinar; rodents; medial geniculate; suprageniculate
Somatosensory cortices of adult primates reactivate over time after sensory loss. The time course and the neural mechanisms underlying the cortical reactivation are not well understood. Here we report that longitudinal high-resolution fMRI studies on anesthetized squirrel monkeys revealed dynamic reorganizations of digit activations in area 3b, within two months after severely disrupting afferent inputs by dorsal column section. We found that digit regions where inputs were severely disrupted exhibited fMRI tactile responses. Reorganization was characterized by an early moving away phase, and a late returning phase, as indicated by spatial shifts of individual digit activation centers in relation to the pre-lesion activation sites. Subsequent optical imaging studies confirmed fMRI activations, and dense microelectrode penetrations identified weak neuronal activity at the reactivated sites. Activation zones detected by fMRI and optical imaging were significantly larger in input-deprived than normal input single digit regions, and were larger than regions defined by neuronal spiking activity. This study captures the dynamic reorganization of digit representations following dorsal column lesions, and reveals differences between activity imaging and microelectrode recording maps. Our observations suggest that subthreshold activity plays an important role in the reactivation of deafferented cortex, and could promote behavioral recovery.
functional MRI; primates; primary somatosensory cortex; spinal cord injury; reaching; touch
Currently, we lack consensus regarding the organization along the anterior border of dorsomedial V2 in primates. Previous studies suggest that this region could be either the dorsomedial area, characterized by both an upper and a lower visual field representation, or the dorsal aspect of area V3, which only contains a lower visual field representation. We examined these proposals by using optical imaging of intrinsic signals to investigate this region in the prosimian galago (Otole-mur garnettii). Galagos represent the prosimian radiation of surviving primates; cortical areas that bear strong resemblances across members of primates provide a strong argument for their early origin and conserved existence. Based on our mapping of horizontal and vertical meridian representations, visuotopy, and orientation preference, we find a clear lower field representation anterior to dorsal V2 but no evidence of any upper field representation. We also show statistical differences in orientation preference patches between V2 and V3. We additionally supplement our imaging results with electrode array data that reveal differences in the average spatial frequency preference, average temporal frequency preference, and sizes of the receptive fields between V1, V2, and V3. The lack of upper visual field representation along with the differences between the neighboring visual areas clearly distinguish the region anterior to dorsal V2 from earlier visual areas and argue against a DM that lies along the dorsomedial border of V2. We submit that the region of the cortex in question is the dorsal aspect of V3, thus strengthening the possibility that V3 is conserved among primates.
V3; galago; imaging; electrode; DM; orientation