Travis Meyer

Statistical learning of visual transitions in monkey inferotemporal cortex

One of the most fundamental functions of the brain is to predict upcoming events on the basis of the recent past. A closely related function is to signal when a prediction has been violated. The identity of the brain regions that mediate these functions is not known. We set out to determine whether they are implemented at the level of single neurons in the visual system. We gave monkeys prolonged exposure to pairs of images presented in fixed sequence so that each leading image became a strong predictor for the corresponding trailing image. We then monitored the responses of neurons in the inferotemporal cortex to image sequences that obeyed or violated the transitional rules imposed during training. Inferotemporal neurons exhibited a transitional surprise effect, responding much more strongly to unpredicted transitions than to predicted transitions. Thus, neurons even in the visual system make experience-based predictions and react when they fail.

Stimulus Selectivity in Dorsal and Ventral Prefrontal Cortex after Training in Working Memory Tasks

The prefrontal cortex is known to represent different types of information in working memory. Contrasting theories propose that the dorsal and ventral regions of the lateral prefrontal cortex are innately specialized for the representation of spatial and nonspatial information, respectively (Goldman-Rakic, 1996), or that the two regions are shaped by the demands of cognitive tasks imposed on them (Miller, 2000). To resolve this issue, we recorded from neurons in the two regions, before and at multiple stages of training monkeys on visual working memory tasks. Before training, substantial functional differences were present between the two regions. Dorsal prefrontal cortex exhibited higher overall responsiveness to visual stimuli and higher selectivity for spatial information. After training, stimulus selectivity generally decreased, although dorsal prefrontal cortex retained higher spatial selectivity regardless of task performed. Ventral prefrontal cortex appeared to be affected to a greater extent by the nature of the task. Our results indicate that regional specialization for stimulus selectivity is present in the primate prefrontal cortex regardless of training. Dorsal areas of the prefrontal cortex are inherently organized to represent spatial information, and training has little influence on this spatial bias. Ventral areas are biased toward nonspatial information, although they are more influenced by training both in terms of activation and changes in stimulus selectivity.

Comparison of neural activity related to working memory in primate dorsolateral prefrontal and posterior parietal cortex.

Neurons in a distributed network of cortical and subcortical areas continue to discharge after the presentation and disappearance of stimuli, providing a neural correlate for working memory. While it is thought that the prefrontal cortex plays a central role in this network, the relative contributions of other brain areas are not as well understood. In order to compare the contributions of the dorsolateral prefrontal and posterior parietal cortex, we recorded neurophysiological activity in monkeys trained to perform two different visuo-spatial working memory tasks: a Match/Nonmatch task, and a Spatial Delayed-Match-to-Sample Task. Neurons in both areas exhibited discharges in the delay periods of the tasks that could be classified in two forms. Sustained discharges persisted after the presentation of a stimulus in the receptive field with a constant or declining rate. Anticipatory responses increased in rate during the delay period, often appearing after presentation of a stimulus out of the receptive field. Despite similarities, we uncovered distinct differences between patterns of delay period in each brain area. Only in the prefrontal cortex sustained responses related to the original stimulus survived presentation of a second stimulus, in the context of the Match/Nonmatch task. Our results provide insights on the nature of processing in two areas active during working memory, and on the unique role of the prefrontal cortex in memory maintenance.

Changes in Prefrontal Neuronal Activity after Learning to Perform a Spatial Working Memory Task

The prefrontal cortex is considered essential for learning to perform cognitive tasks though little is known about how the representation of stimulus properties is altered by learning. To address this issue, we recorded neuronal activity in monkeys before and after training on a task that required visual working memory. After the subjects learned to perform the task, we observed activation of more prefrontal neurons and increased activity during working memory maintenance. The working memory-related increase in firing rate was due mostly to regular-spiking putative pyramidal neurons. Unexpectedly, the selectivity of neurons for stimulus properties and the ability of neurons to discriminate between stimuli decreased as the information about stimulus properties was apparently present in neural firing prior to training and neuronal selectivity degraded after training in the task. The effect was robust and could not be accounted for by differences in sampling sites, selection of neurons, level of performance, or merely the elapse of time. The results indicate that, in contrast to the effects of perceptual learning, mastery of a cognitive task degrades the apparent stimulus selectivity as neurons represent more abstract information related to the task. This effect is countered by the recruitment of more neurons after training.

A software solution for the control of visual behavioral experimentation

Psychophysical and neurophysiological research requires precise control of experimental devices for the purpose of delivering stimuli and monitoring behavioral and neural responses. This has previously been accomplished by complex, often proprietary, programmable systems, interfacing with a limited range of hardware. We have developed a software solution entirely within the Matlab environment that can achieve high-speed control of experimental and behavioral variables. We make this Wake-Forest Visual Experimentation (WaVE) software freely available under the GNU public license, and demonstrate how to customize it to individual laboratory needs. WaVE takes advantage of existing Matlab libraries and toolboxes to present visual stimuli, collect experimental data, update behavioral variables, and communicate with other computers. Although we have developed it for use in a Windows-based Personal Computer, the portability of the Matlab code makes possible its customization for use in a variety of other systems. We present simulation results showing sub-millisecond sampling rate and updating precision, running on single-processor, desktop PCs. The WaVE software offers a simple, flexible and powerful solution that compares favorably with many of its costly alternatives.

Neural Correlates of a Decision Variable Before Learning to Perform a Match/Non-Match Task

The lateral prefrontal cortex plays an important role in working memory and decision-making, although little is known about how neural correlates of these functions are shaped by learning. To understand the effect of learning on the neuronal representation of decision-making, we recorded single neurons from the lateral prefrontal cortex of monkeys before and after they were trained to judge whether two stimuli appeared at matching spatial locations. After training, and in agreement with previous studies, a population of neurons exhibited activity that was modulated depending on whether the second stimulus constituted a match or not, which had predictive ability for the monkeys choice. However, even before training, prefrontal neurons displayed modulation depending on the match or non-match status of a stimulus, with approximately equal percentages of neurons preferring a match or a non-match. The difference in firing rate and discriminability for match and non-match stimuli before training was of comparable magnitude as that after training. Changes observed after training involved an increase in the percentage of neurons exhibiting this effect, a greater proportion of neurons preferring non-match stimuli, and a greater percentage of neurons representing information about the first stimulus during the presentation of the second stimulus. Our results suggest that the neuronal activity representing some match/non-match judgments is present in the lateral prefrontal cortex even when subjects are not required to perform a comparison and before any training.

Image familiarization sharpens response dynamics of neurons in inferotemporal cortex

Repeated viewing of an image over days and weeks induces a marked reduction in the strength with which neurons in monkey inferotemporal cortex respond to it. The processing advantage that attaches to this reduction is unknown. One possibility is that truncation of the response to a familiar image leaves neurons in a state of readiness to respond to ensuing images and thereby enhances their ability to track rapidly changing displays. We explored this possibility by assessing neuronal responses to familiar and novel images in rapid serial visual displays. Inferotemporal neurons responded more strongly to familiar than to novel images in such displays. The effect was stronger among putative inhibitory neurons than among putative excitatory neurons. A comparable effect occurred at the level of the scalp potential in humans. We conclude that long-term familiarization sharpens the response dynamics of neurons in both monkey and human extrastriate visual cortex.

Differences in Intrinsic Functional Organization Between Dorsolateral Prefrontal and Posterior Parietal Cortex

The dorsolateral prefrontal and posterior parietal cortex are 2 components of the cortical network controlling attention, working memory, and executive function. Little is known about how the anatomical organization of the 2 areas accounts for their functional specialization. In order to address this question, we examined the strength of intrinsic functional connectivity between neurons sampled in each area by means of cross-correlation analyses of simultaneous recordings from monkeys trained to perform working memory tasks. In both areas, effective connectivity declined as a function of distance between neurons. However, the strength of effective connectivity was higher overall and more localized over short distances in the posterior parietal than the prefrontal cortex. The difference in connectivity strength between the 2 areas could not be explained by differences in firing rate or selectivity for the stimuli and task events, it was present when the fixation period alone was analyzed, and according to simulation results, was consistent with a systematic difference either in the strength or in the relative numbers of shared inputs between neurons. Our results indicate that the 2 areas are characterized by unique intrinsic functional organization, consistent with known differences in their response patterns during working memory.

Prediction suppression in monkey inferotemporal cortex depends on the conditional probability between images

When monkeys view two images in fixed sequence repeatedly over days and weeks, neurons in area TE of the inferotemporal cortex come to exhibit prediction suppression. The trailing image elicits only a weak response when presented following the leading image that preceded it during training. Induction of prediction suppression might depend either on the contiguity of the images, as determined by their co-occurrence and captured in the measure of joint probability P(A,B), or on their contingency, as determined by their correlation and as captured in the measures of conditional probability P(A|B) and P(B|A). To distinguish between these possibilities, we measured prediction suppression after imposing training regimens that held P(A,B) constant but varied P(A|B) and P(B|A). We found that reducing either P(A|B) or P(B|A) during training attenuated prediction suppression as measured during subsequent testing. We conclude that prediction suppression depends on contingency, as embodied in the predictive relations between the images, and not just on contiguity, as embodied in their co-occurrence.

Prediction suppression and surprise enhancement in monkey inferotemporal cortex

Exposing monkeys, over the course of days and weeks, to pairs of images presented in fixed sequence, so that each leading image becomes a predictor for the corresponding trailing image, affects neuronal visual responsiveness in area TE. At the end of the training period, neurons respond relatively weakly to a trailing image when it appears in a trained sequence and, thus, confirms prediction, whereas they respond relatively strongly to the same image when it appears in an untrained sequence and, thus, violates prediction. This effect could arise from prediction suppression (reduced firing in response to the occurrence of a probable event) or surprise enhancement (elevated firing in response to the omission of a probable event). To identify its cause, we compared firing under the prediction-confirming and prediction-violating conditions to firing under a prediction-neutral condition. The results provide strong evidence for prediction suppression and limited evidence for surprise enhancement.NEW & NOTEWORTHY In predictive coding models of the visual system, neurons carry signed prediction error signals. We show here that monkey inferotemporal neurons exhibit prediction-modulated firing, as posited by these models, but that the signal is unsigned. The response to a prediction-confirming image is suppressed, and the response to a prediction-violating image may be enhanced. These results are better explained by a model in which the visual system emphasizes unpredicted events than by a predictive coding model.