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1.  Variance predicts salience in central sensory processing 
eLife  null;3:e03722.
Information processing in the sensory periphery is shaped by natural stimulus statistics. In the periphery, a transmission bottleneck constrains performance; thus efficient coding implies that natural signal components with a predictably wider range should be compressed. In a different regime—when sampling limitations constrain performance—efficient coding implies that more resources should be allocated to informative features that are more variable. We propose that this regime is relevant for sensory cortex when it extracts complex features from limited numbers of sensory samples. To test this prediction, we use central visual processing as a model: we show that visual sensitivity for local multi-point spatial correlations, described by dozens of independently-measured parameters, can be quantitatively predicted from the structure of natural images. This suggests that efficient coding applies centrally, where it extends to higher-order sensory features and operates in a regime in which sensitivity increases with feature variability.
eLife digest
Our senses are constantly bombarded by sights and sounds, but the capacity of the brain to process all these inputs is finite. The stimuli that contain the most useful information must therefore be prioritized for processing by the brain to ensure that we build up as complete a picture as possible of the world around us. However, the strategy that the brain uses to select certain stimuli—or certain features of stimuli—for processing at the expense of others is unclear.
Hermundstad et al. have now provided new insights into this process by analyzing how humans respond to artificial stimuli that contain controllable mixtures of features that found in natural stimuli. To do this, Hermundstad et al. selected photographs of the natural world, and measured the brightness of individual pixels. After adjusting images in a way that mimics the human retina, the brightest 50% of the pixels in each photograph were colored white and the remaining 50% were colored black.
Hermundstad et al. then used statistical techniques to calculate the degree to which the color of pixels could be used to predict the color of their neighbors. In this way, it was possible to calculate the amount of variation throughout the images, and then make computer-generated images in which pixel colorings were more or less predictable than in the natural images.
Volunteers then performed a task in which they had to locate a computer-generated pattern against a background of random noise. The volunteers were able to locate this target most easily when it contained the same kinds of patterns and features that were meaningful about natural images.
While this shows that the brain is adapted to prioritize features that are more informative about the natural world, understanding exactly how the brain implements this strategy remains a challenge.
PMCID: PMC4271187  PMID: 25396297
natural scene statistics; neural coding; visual cortex; normative theories; human
2.  Common resting brain dynamics indicate a possible mechanism underlying zolpidem response in severe brain injury 
eLife  2013;2:e01157.
Zolpidem produces paradoxical recovery of speech, cognitive and motor functions in select subjects with severe brain injury but underlying mechanisms remain unknown. In three diverse patients with known zolpidem responses we identify a distinctive pattern of EEG dynamics that suggests a mechanistic model. In the absence of zolpidem, all subjects show a strong low frequency oscillatory peak ∼6–10 Hz in the EEG power spectrum most prominent over frontocentral regions and with high coherence (∼0.7–0.8) within and between hemispheres. Zolpidem administration sharply reduces EEG power and coherence at these low frequencies. The ∼6–10 Hz activity is proposed to arise from intrinsic membrane properties of pyramidal neurons that are passively entrained across the cortex by locally-generated spontaneous activity. Activation by zolpidem is proposed to arise from a combination of initial direct drug effects on cortical, striatal, and thalamic populations and further activation of underactive brain regions induced by restoration of cognitively-mediated behaviors.
eLife digest
Some individuals who experience severe brain damage are left with disorders of consciousness. While they can appear to be awake, these individuals lack awareness of their surroundings and cannot respond to events going on around them. Few treatments are available, but a minority of patients show striking improvements in speech, alertness and movement in response to the sleeping pill zolpidem.
Although the idea of a sleeping pill increasing consciousness is paradoxical, it is possible that in patients with impaired consciousness, zolpidem reduces the activity of an area of the brain that would otherwise inhibit activity in other regions of the brain. However, the precise mechanisms by which zolpidem increases consciousness in these patients, and the reasons why only a minority of individuals respond, are unknown.
Now, Williams et al. have used electrodes attached to the scalp to measure changes in brain activity in three patients known to respond to zolpidem. These measurements showed that before the drug was taken, there were two important differences between the brain activity of the patients and that of healthy subjects: first, the patients showed brain waves of a lower frequency than any seen in healthy subjects; second, these brain waves were much more synchronized than brain activity in healthy individuals. After taking zolpidem, this synchronicity was reduced and all of the patients also showed an increase in higher frequency brain waves.
Based on the effects of zolpidem on electrical activity throughout the brain, Williams et al. propose a new model to explain the therapeutic action of the drug in some minimally conscious patients. If the correlation between brain waves and zolpidem response holds up in future studies, this relation could be used to predict which patients might benefit from the drug. A better understanding of these processes should also help us to understand, diagnose and develop new treatments for disorders of consciousness.
PMCID: PMC3833342  PMID: 24252875
Consciousness; central thalamus; striatum; GABA-A; arousal; anesthesia; Human
3.  Responses to Orientation Discontinuities in V1 and V2: Physiological Dissociations and Functional Implications 
The Journal of Neuroscience  2014;34(10):3559-3578.
Segmenting the visual image into objects is a crucial stage of visual processing. Object boundaries are typically associated with differences in luminance, but discontinuities in texture also play an important role. We showed previously that a subpopulation of neurons in V2 in anesthetized macaques responds to orientation discontinuities parallel to their receptive field orientation. Such single-cell responses could be a neurophysiological correlate of texture boundary detection. Neurons in V1, on the other hand, are known to have contextual response modulations such as iso-orientation surround suppression, which also produce responses to orientation discontinuities. Here, we use pseudorandom multiregion grating stimuli of two frame durations (20 and 40 ms) to probe and compare texture boundary responses in V1 and V2 in anesthetized macaque monkeys. In V1, responses to texture boundaries were observed for only the 40 ms frame duration and were independent of the orientation of the texture boundary. However, in transient V2 neurons, responses to such texture boundaries were robust for both frame durations and were stronger for boundaries parallel to the neuron's preferred orientation. The dependence of these processes on stimulus duration and orientation indicates that responses to texture boundaries in V2 arise independently of contextual modulations in V1. In addition, because the responses in transient V2 neurons are sensitive to the orientation of the texture boundary but those of V1 neurons are not, we suggest that V2 responses are the correlate of texture boundary detection, whereas contextual modulation in V1 serves other purposes, possibly related to orientation “pop-out.”
PMCID: PMC3942574  PMID: 24599456
contextual modulation; cue invariance; pop-out; spatial nonlinearities; surround suppression; texture segmentation
4.  Post-stroke apathy and hypersomnia lead to worse outcomes from acute rehabilitation 
Translational stroke research  2013;5(2):292-300.
Apathy and hypersomnia occur after stroke and, by definition, reduce participation in rehabilitation, but their effect on outcome from acute rehabilitation is not known. We performed a retrospective review of 213 patients admitted to a stroke-specialized acute rehabilitation unit in the United States. All patients had ischemic or hemorrhagic stroke, and no dementia or dependence on others pre-stroke. We diagnosed apathy and hypersomnia using standardized documentation by treating therapists. We used multiple regression analysis to control for overall impairment (combination of strength, cognitive and sensory measures), age, time since stroke, and stroke type (ischemic or hemorrhagic).
44 (21%) of patients had persistent apathy, and 12 (5.6%) had persistent hypersomnia. Both groups were more impaired in cognition, sustained attention, and more likely to be treated for depression. Patients with apathy were 2.4 times more likely to go to a nursing home, and had discharge FIM scores 12 points below the mean. Patients with hypersomnia were 10 times more likely to go to a nursing home, and had discharge FIM scores 16 points below the mean. These findings indicate that studies to prospectively define these clinical factors and potential confounds using standardized tools are indicated, and if confirmed, justify studies to identify these patients early and develop targeted interventions.
PMCID: PMC3955405  PMID: 24323716
apathy; hypersomnia; stroke; rehabilitation
5.  The statistics of local motion signals in naturalistic movies 
Journal of Vision  2014;14(4):10.
Extraction of motion from visual input plays an important role in many visual tasks, such as separation of figure from ground and navigation through space. Several kinds of local motion signals have been distinguished based on mathematical and computational considerations (e.g., motion based on spatiotemporal correlation of luminance, and motion based on spatiotemporal correlation of flicker), but little is known about the prevalence of these different kinds of signals in the real world. To address this question, we first note that different kinds of local motion signals (e.g., Fourier, non-Fourier, and glider) are characterized by second- and higher-order correlations in slanted spatiotemporal regions. The prevalence of local motion signals in natural scenes can thus be estimated by measuring the extent to which each of these correlations are present in space-time patches and whether they are coherent across spatiotemporal scales. We apply this technique to several popular movies. The results show that all three kinds of local motion signals are present in natural movies. While the balance of the different kinds of motion signals varies from segment to segment during the course of each movie, the overall pattern of prevalence of the different kinds of motion and their subtypes, and the correlations between them, is strikingly similar across movies (but is absent from white noise movies). In sum, naturalistic movies contain a diversity of local motion signals that occur with a consistent prevalence and pattern of covariation, indicating a substantial regularity of their high-order spatiotemporal image statistics.
PMCID: PMC3987513  PMID: 24732243
local motion signals; non-Fourier motion; glider motion; spatiotemporal image statistics
6.  Cannabinoid Neuromodulation in the Adult Early Visual Cortex 
PLoS ONE  2014;9(2):e87362.
Sensory processing is an active process involving the interaction of ongoing cortical activity with incoming stimulus information. However, the modulators and circuits involved in this interaction are incompletely understood. One potential candidate is the cannabinoid-signaling system, which is known to modulate the dynamics of cortical networks. Here, we show that in the primate primary and secondary visual cortices, the cannabinoid CP55940 modulates not only population dynamics but also influences the dynamics of the stimulus-response relationship of individual neurons. At the population level, CP55940 decreases EEG power, LFP power, and LFP coherence. At the single-neuron level, intrinsic spike train dynamics appear relatively unchanged, but visual receptive fields are altered: CP55940 induced an overall delay and broadening of the temporal component of V1 and V2 spatiotemporal receptive fields. Our findings provide neurophysiologic evidence for a link between cannabinoid-signaling, network dynamics and the function of a canonical cortical circuit.
PMCID: PMC3929390  PMID: 24586271
7.  Spike train metrics 
Current opinion in neurobiology  2005;15(5):585-592.
Quantifying similarity and dissimilarity of spike trains is an important requisite for understanding neural codes. Spike metrics constitute a class of approaches to this problem. In contrast to most signal-processing methods, spike metrics operate on time series of all-or-none events, and are, thus, particularly appropriate for extracellularly recorded neural signals. The spike metric approach can be extended to multineuronal recordings, mitigating the ‘curse of dimensionality’ typically associated with analyses of multivariate data. Spike metrics have been usefully applied to the analysis of neural coding in a variety of systems, including vision, audition, olfaction, taste and electric sense.
PMCID: PMC2713191  PMID: 16140522
8.  VEPs elicited by local correlations and global symmetry: characteristics and interactions 
Vision research  2007;47(16):2212-2222.
Psychophysical and fMRI studies have indicated that visual processing of global symmetry has distinctive scaling properties, and proceeds more slowly than analysis of contrast, spatial frequency, and texture. We therefore undertook a visual evoked potential (VEP) study to directly compare the dynamics of symmetry and texture processing, and to determine the extent to which they interact.
Stimuli consisted of interchange between structured and random black-and-white checkerboard stimuli. For symmetry, structured stimuli were colored with 2-fold symmetry (horizontal or vertical mirror), 4-fold symmetry (both mirror axes), and 8-fold symmetry (oblique mirror axes added). For texture, structured stimuli were colored according to the “even” isodipole texture (Julesz, Gilbert & Victor, 1978). Thus, all stimuli had the same contrast, and check size, but differed substantially in correlation structure.
To separate components of the VEP related to symmetry and texture from components that could be generated by local luminance and contrast changes, we extracted the odd-harmonic components of the VEP (recorded at Cz-Oz, Cz-O1, Cz-O2, Cz-Pz) elicited by structured-random interchange.
Responses to symmetry were largest for the 8-fold patterns, and progressively smaller for 4-fold, vertical, and horizontal symmetry patterns. 8-fold patterns were therefore used in the remainder of the study. The symmetry response is shifted to larger checks and lower temporal frequencies compared to the response to texture, and its temporal tuning is broader. Processing of symmetry makes use of neural mechanisms with larger receptive fields, and slower, more sustained temporal tuning characteristics than those involved in the analysis of texture.
Sparse stimuli were used to dissociate check size and check density. VEP responses to sparse symmetry stimuli showed that there is no difference between 1st and 2nd order symmetry for densities less than 12.5%. We discuss these findings in relation to local and global visual processes.
PMCID: PMC2041857  PMID: 17604074
Symmetry; texture; visual evoked potentials; isodipole; form vision
9.  Information Processing in the Parabrachial Nucleus of the Pons 
As the second synapse in the central gustatory pathway of the rodent, the parabrachial nucleus of the pons (PbN) receives information about taste stimuli directly from the nucleus of the solitary tract (NTS). Data show that NTS cells amplify taste responses before transmitting taste-related signals to the PbN. NTS cells of varied response profiles send converging input to PbN cells, though input from NTS cells with similar profiles is more effective at driving PbN responses. PbN cells follow NTS input for the first 3 s of taste stimulation for NaCl, HCl, and quinine, but are driven in cyclic bursts throughout the response interval for sucrose. Analyses of the temporal characteristics of NTS and PbN responses show that both structures use temporal coding with equal effectiveness to identify taste quality. Thus, the NTS input to the PbN is comprehensive, in that PbN cells receive NTS input that could support broad sensitivity, systematic, in that the time course of PbN firing patterns depend reliably on the tastant, and efficient, in that information from the NTS is preserved as it is communicated across structures. Comparisons of NTS and PbN taste responses in rats form the basis for our speculation that in primates, where the central gustatory pathway does not synapse in the PbN, the function of the PbN in taste processing may have been incorporated into that of the NTS.
PMCID: PMC3759149  PMID: 19686160
taste; parabrachial pons; temporal coding
10.  Information theory in neuroscience 
PMCID: PMC3736735  PMID: 21279429
12.  Perception of second- and third-order orientation signals and their interactions 
Journal of Vision  2013;13(4):21.
Orientation signals, which are crucial to many aspects of visual function, are more complex and varied in the natural world than in the stimuli typically used for laboratory investigation. Gratings and lines have a single orientation, but in natural stimuli, local features have multiple orientations, and multiple orientations can occur even at the same location. Moreover, orientation cues can arise not only from pairwise spatial correlations, but from higher-order ones as well. To investigate these orientation cues and how they interact, we examined segmentation performance for visual textures in which the strengths of different kinds of orientation cues were varied independently, while controlling potential confounds such as differences in luminance statistics. Second-order cues (the kind present in gratings) at different orientations are largely processed independently: There is no cancellation of positive and negative signals at orientations that differ by 45°. Third-order orientation cues are readily detected and interact only minimally with second-order cues. However, they combine across orientations in a different way: Positive and negative signals largely cancel if the orientations differ by 90°. Two additional elements are superimposed on this picture. First, corners play a special role. When second-order orientation cues combine to produce corners, they provide a stronger signal for texture segregation than can be accounted for by their individual effects. Second, while the object versus background distinction does not influence processing of second-order orientation cues, this distinction influences the processing of third-order orientation cues.
PMCID: PMC3616601  PMID: 23532909
high-order statistics; visual textures; perceptual metric; corner
13.  Temporal Encoding of Spatial Information during Active Visual Fixation 
Current Biology  2012;22(6):510-514.
Humans and other species continually perform microscopic eye movements, even when attending to a single point [1-3]. These movements, which include microscopic drifts and microsaccades, are under control of the oculomotor system [2, 4, 5], elicit strong responses throughout the visual system [6-11], and have been thought to serve important functions [12-16]. The influence of these fixational eye movements on the acquisition and neural processing of visual information remains unknown. Here, we show that during viewing of natural scenes, microscopic eye movements carry out a crucial information-processing step: they remove predictable correlations in natural scenes by equalizing the spatial power of the retinal image within the frequency range of ganglion cells' peak sensitivity. This transformation, which had been attributed to center-surround receptive field organization [17-19], occurs prior to any neural processing, and reveals a form of matching between the statistics of natural images and those of normal eye movements. We further show that the combined effect of microscopic eye movements and retinal receptive field organization is to convert spatial luminance discontinuities into synchronous firing events, thus beginning the process of edge extraction. In sum, our results show that microscopic eye movements are fundamental to two goals of early visual processing —redundancy reduction [20, 21] and feature extraction— and, thus, that neural representations are intrinsically sensory-motor from the very first processing stages.
PMCID: PMC3332095  PMID: 22342751
14.  Dipole characterization of single neurons from their extracellular action potentials 
The spatial variation of the extracellular action potentials (EAP) of a single neuron contains information about the size and location of the dominant current source of its action potential generator, which is typically in the vicinity of the soma. Using this dependence in reverse in a three-component realistic probe + brain + source model, we solved the inverse problem of characterizing the equivalent current source of an isolated neuron from the EAP data sampled by an extracellular probe at multiple independent recording locations. We used a dipole for the model source because there is extensive evidence it accurately captures the spatial roll-off of the EAP amplitude, and because, as we show, dipole localization, beyond a minimum cell-probe distance, is a more accurate alternative to approaches based on monopole source models. Dipole characterization is separable into a linear dipole moment optimization where the dipole location is fixed, and a second, nonlinear, global optimization of the source location. We solved the linear optimization on a discrete grid via the lead fields of the probe, which can be calculated for any realistic probe + brain model by the finite element method. The global source location was optimized by means of Tikhonov regularization that jointly minimizes model error and dipole size. The particular strategy chosen reflects the fact that the dipole model is used in the near field, in contrast to the typical prior applications of dipole models to EKG and EEG source analysis. We applied dipole localization to data collected with stepped tetrodes whose detailed geometry was measured via scanning electron microscopy. The optimal dipole could account for 96% of the power in the spatial variation of the EAP amplitude. Among various model error contributions to the residual, we address especially the error in probe geometry, and the extent to which it biases estimates of dipole parameters. This dipole characterization method can be applied to any recording technique that has the capabilities of taking multiple independent measurements of the same single units.
PMCID: PMC3274615  PMID: 21667156
Multisite recording; Inverse problem; Passive conductor model; Lead field theory; Finite element method (FEM)
15.  Taste Coding in the Nucleus of the Solitary Tract of the Awake, Freely Licking Rat 
It is becoming increasingly clear that the brain processes sensory stimuli differently according to whether they are passively or actively acquired, and these differences can be seen early in the sensory pathway. In the nucleus of the solitary tract (NTS), the first relay in the central gustatory neuraxis, a rich variety of sensory inputs generated by active licking converge. Here we show that taste responses in the NTS reflect these interactions. Experiments consisted of recordings of taste-related activity in the NTS of awake rats as they freely licked exemplars of the five basic taste qualities (sweet, sour, salty, bitter, umami). Nearly all taste-responsive cells were broadly tuned across taste qualities. A subset responded to taste with long latencies (>1.0 s), suggesting the activation of extra-oral chemoreceptors. Analyses of the temporal characteristics of taste responses showed that spike timing conveyed significantly more information than spike count alone in almost half of NTS cells, as in anesthetized rats, but with less information per cell. In addition to taste-responsive cells, the NTS contains cells that synchronize with licks. Since the lick pattern per se can convey information, these cells may collaborate with taste-responsive cells to identify taste quality. Other cells become silent during licking. These latter “anti-lick” cells show a surge in firing rate predicting the beginning and signaling the end of a lick bout. Collectively, the data reveal a complex array of cell types in the NTS, only a portion of which include taste-responsive cells, which work together to acquire sensory information.
PMCID: PMC3427930  PMID: 22855799
16.  Determination of awareness in patients with severe brain injury using EEG power spectral analysis 
To determine whether EEG spectral analysis could be used to demonstrate awareness in patients with severe brain injury.
We recorded EEG from healthy controls and three patients with severe brain injury, ranging from minimally conscious state (MCS) to locked-in-state (LIS), while they were asked to imagine motor and spatial navigation tasks. We assessed EEG spectral differences from 4 to 24 Hz with univariate comparisons (individual frequencies) and multivariate comparisons (patterns across the frequency range).
In controls, EEG spectral power differed at multiple frequency bands and channels during performance of both tasks compared to a resting baseline. As patterns of signal change were inconsistent between controls, we defined a positive response in patient subjects as consistent spectral changes across task performances. One patient in MCS and one in LIS showed evidence of motor imagery task performance, though with patterns of spectral change different from the controls.
EEG power spectral analysis demonstrates evidence for performance of mental imagery tasks in healthy controls and patients with severe brain injury.
EEG power spectral analysis can be used as a flexible bedside tool to demonstrate awareness in brain-injured patients who are otherwise unable to communicate.
PMCID: PMC3162107  PMID: 21514214
Consciousness; EEG spectral analysis; motor imagery; traumatic brain injury; locked-in-state; minimally conscious state
17.  Local image statistics: maximum-entropy constructions and perceptual salience 
The space of visual signals is high-dimensional and natural visual images have a highly complex statistical structure. While many studies suggest that only a limited number of image statistics are used for perceptual judgments, a full understanding of visual function requires analysis not only of the impact of individual image statistics, but also, how they interact. In natural images, these statistical elements (luminance distributions, correlations of low and high order, edges, occlusions, etc.) are intermixed, and their effects are difficult to disentangle. Thus, there is a need for construction of stimuli in which one or more statistical elements are introduced in a controlled fashion, so that their individual and joint contributions can be analyzed. With this as motivation, we present algorithms to construct synthetic images in which local image statistics—including luminance distributions, pair-wise correlations, and higher-order correlations—are explicitly specified and all other statistics are determined implicitly by maximum-entropy. We then apply this approach to measure the sensitivity of the human visual system to local image statistics and to sample their interactions.
PMCID: PMC3396046  PMID: 22751397
18.  Detecting symmetry and faces: Separating the tasks and identifying their interactions 
Face and symmetry processing have common characteristics, and several lines of evidence suggest they interact. To characterize their relationship and possible interactions, in the present study we created a novel library of images in which symmetry and face-likeness were manipulated independently. Participants identified the target that was most symmetric among distractors of equal face-likeness (Experiment 1) and identified the target that was most face-like among distractors of equal symmetry (Experiment 2). In Experiment 1, we found that symmetry judgments improved when the stimuli were more face-like. In Experiment 2, we found a more complex interaction: Image symmetry had no effect on detecting frontally viewed faces, but worsened performance for nonfrontally viewed faces. There was no difference in performance for upright versus inverted images, suggesting that these interactions occurred on the parts-based level. In sum, when symmetry and face-likeness are independently manipulated, we find that each influences the perception of the other, but the nature of the interactions differs.
PMCID: PMC3392169  PMID: 22419373
Faces; Symmetry; Vision; Inversion effect
20.  Information-geometric measure of 3-neuron firing patterns characterizes scale-dependence in cortical networks 
To understand the functional connectivity of neural networks, it is important to develop simple and incisive descriptors of multineuronal firing patterns. Analysis at the pairwise level has proven to be a powerful approach in the retina, but it may not suffice to understand complex cortical networks. Here we address the problem of describing interactions among triplets of neurons. We consider two approaches: an information-geometric measure (Amari, 2001), which we call the “strain,” and the Kullback-Leibler divergence. While both approaches can be used to assess whether firing patterns differ from those predicted by a pairwise maximum-entropy model, the strain provides additional information. Specifically, when the observed firing patterns differ from those predicted by a pairwise model, the strain indicates the nature of this difference – whether there is an excess or a deficit of synchrony – while the Kullback-Leibler divergence only indicates the magnitude of the difference. We show that the strain has technical advantages, including ease of calculation of confidence bounds and bias, and robustness to the kinds of spike-sorting errors associated with tetrode recordings.
We demonstrate the biological importance of these points via an analysis of multineuronal firing patterns in primary visual cortex. There is a striking scale-dependent behavior of triplet firing patterns: deviations from the pairwise model are substantial when the neurons are within 300 microns of each other, and negligible when they are at a distance of > 600 microns. The strain identifies a consistent pattern to these interactions: when triplet interactions are present, the strain is nearly always negative, indicating that there is less synchrony than would be expected from the pairwise interactions alone.
PMCID: PMC2974058  PMID: 20635129
Maximum entropy; Pairwise model; Multineuron; Synchrony; Information geometry
21.  Sparse coding and high-order correlations in fine-scale cortical networks 
Nature  2010;466(7306):617-621.
Connectivity in the cortex is organized at multiple scales 1-5, suggesting that scale-dependent correlated activity is particularly important for understanding the behavior of sensory cortices and their function in stimulus encoding. Here, we analyze the scale-dependent structure of cortical interactions by using maximum entropy models 6-9 to characterize multiple-tetrode recordings from primary visual cortex of anesthetized monkeys (Macaca mulatta). We compare the properties of firing patterns among local clusters of neurons (<300 microns) with neurons separated by larger distances (600-2500 microns). We find that local firing patterns are distinctive: while multi-neuronal firing patterns at larger distances can be predicted by pairwise interactions, patterns within local clusters often show evidence of high-order correlations. Surprisingly, these local correlations are flexible and rapidly reorganized by visual input. While they modestly reduce the amount of information that a cluster conveys, they also modify the format of this information, creating sparser codes by increasing the periods of total quiescence, and concentrating information into briefer periods of common activity. These results imply a hierarchical organization of neuronal correlations: simple pairwise correlations link neurons over scales of tens to hundreds of minicolumns, but on the scale of a few minicolumns, ensembles of neurons form complex subnetworks whose moment-to-moment effective connectivity is dynamically reorganized by the stimulus.
PMCID: PMC2912961  PMID: 20601940
22.  Symmetry breakdown in the ON and OFF pathways of the retina at night: functional implications 
Several recent studies have shown that the ON and OFF channels of the visual system are not simple mirror images of each other, that their response characteristics are asymmetric (Chichilnisky and Kalmar, 2002; Sagdullaev and McCall, 2005). How the asymmetries bear on visual processing is not well understood. Here we show that ON and OFF ganglion cells show a strong asymmetry in their temporal adaptation to photopic (day) and scotopic (night) conditions and that the asymmetry confers a functional advantage. Under photopic conditions, the ON and OFF ganglion cells show similar temporal characteristics. Under scotopic conditions, the two cell classes diverge – ON cells shift their tuning to low temporal frequencies, while OFF cells continue to respond to high. This difference in processing corresponds to an asymmetry in the natural world, one produced by the Poisson nature of photon capture and persists over a broad range of light levels. This work characterizes a previously unknown divergence in the ON and OFF pathways and its utility to visual processing. Furthermore, the results have implications for downstream circuitry and thus offer new constraints for models of downstream processing, since ganglion cells serve as building blocks for circuits in higher brain areas. For example, if simple cells in visual cortex rely on complementary interactions between the two pathways, such as push-pull interactions (Alonso et al., 2001; Hirsch, 2003), their receptive fields may be radically different under scotopic conditions, when the ON and OFF pathways are out of sync.
PMCID: PMC2940838  PMID: 20668185
Retinal Ganglion Cell; Sensory Neurons; Parallel; Information; Vision; Receptive Field; Population coding
23.  A Bayesian statistical analysis of behavioral facilitation associated with deep brain stimulation 
Journal of neuroscience methods  2009;183(2):267-276.
Deep brain stimulation (DBS) is an established therapy for Parkinson’s Disease and is being investigated as a treatment for chronic depression, obsessive compulsive disorder and for facilitating functional recovery of patients in minimally conscious states following brain injury. For all of these applications, quantitative assessments of the behavioral effects of DBS are crucial to determine whether the therapy is effective and, if so, how stimulation parameters can be optimized. Behavioral analyses for DBS are challenging because subject performance is typically assessed from only a small set of discrete measurements made on a discrete rating scale, the time course of DBS effects is unknown, and between-subject differences are often large. We demonstrate how Bayesian state-space methods can be used to characterize the relationship between DBS and behavior comparing our approach with logistic regression in two experiments: the effects of DBS on attention of a macaque monkey performing a reaction-time task, and the effects of DBS on motor behavior of a human patient in a minimally conscious state. The state-space analysis can assess the magnitude of DBS behavioral facilitation (positive or negative) at specific time points and has important implications for developing principled strategies to optimize DBS paradigms.
PMCID: PMC2743761  PMID: 19576932
deep brain stimulation; state-space models; Bayesian estimation; behavior; model selection; logistic regression
24.  Spike Train Analysis Toolkit: Enabling Wider Application of Information-Theoretic Techniques to Neurophysiology 
Neuroinformatics  2009;7(3):165-178.
Conventional methods widely available for the analysis of spike trains and related neural data include various time- and frequency-domain analyses, such as peri-event and interspike interval histograms, spectral measures, and probability distributions. Information theoretic methods are increasingly recognized as significant tools for the analysis of spike train data. However, developing robust implementations of these methods can be time-consuming, and determining applicability to neural recordings can require expertise. In order to facilitate more widespread adoption of these informative methods by the neuroscience community, we have developed the Spike Train Analysis Toolkit. STAToolkit is a software package which implements, documents, and guides application of several information-theoretic spike train analysis techniques, thus minimizing the effort needed to adopt and use them. This implementation behaves like a typical Matlab toolbox, but the underlying computations are coded in C for portability, optimized for efficiency, and interfaced with Matlab via the MEX framework. STAToolkit runs on any of three major platforms: Windows, Mac OS, and Linux. The toolkit reads input from files with an easy-to-generate text-based, platform-independent format. STAToolkit, including full documentation and test cases, is freely available open source via, maintained as a resource for the computational neuroscience and neuroinformatics communities. Use cases drawn from somatosensory and gustatory neurophysiology, and community use of STAToolkit, demonstrate its utility and scope.
PMCID: PMC2818590  PMID: 19475519
Computational neuroscience; Information theory; Neural coding; Neurodatabases; Data sharing
25.  Responses of V1 Neurons to Two-Dimensional Hermite Functions 
Journal of neurophysiology  2005;95(1):379-400.
Neurons in primary visual cortex are widely considered to be oriented filters or energy detectors that perform one-dimensional feature analysis. The main deviations from this picture are generally thought to include gain controls and modulatory influences. Here we investigate receptive field (RF) properties of single neurons with localized two-dimensional stimuli, the two-dimensional Hermite functions (TDHs). TDHs can be grouped into distinct complete orthonormal bases that are matched in contrast energy, spatial extent, and spatial frequency content but differ in two-dimensional form, and thus can be used to probe spatially specific nonlinearities. Here we use two such bases: Cartesian TDHs, which resemble vignetted gratings and checkerboards, and polar TDHs, which resemble vignetted annuli and dartboards. Of 63 isolated units, 51 responded to TDH stimuli. In 37/51 units, we found significant differences in overall response size (21/51) or apparent RF shape (28/51) that depended on which basis set was used. Because of the properties of the TDH stimuli, these findings are inconsistent with simple feedforward nonlinearities and with many variants of energy models. Rather, they imply the presence of nonlinearities that are not local in either space or spatial frequency. Units showing these differences were present to a similar degree in cat and monkey, in simple and complex cells, and in supragranular, infragranular, and granular layers. We thus find a widely distributed neurophysiological substrate for two-dimensional spatial analysis at the earliest stages of cortical processing. Moreover, the population pattern of tuning to TDH functions suggests that V1 neurons sample not only orientations, but a larger space of two-dimensional form, in an even-handed manner.
PMCID: PMC2927229  PMID: 16148274

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