Yasuko Sugase-Miyamoto

Neuronal Signals in the Monkey Basolateral Amygdala during Reward Schedules

The amygdala is critical for connecting emotional reactions with environmental events. We recorded neurons from the basolateral complex of two monkeys while they performed visually cued schedules of sequential color discrimination trials, with both valid and random cues. When the cues were valid, the visual cue, which was present throughout each trial, indicated how many trials remained to be successfully completed before a reward. Seventy-six percent of recorded neurons showed response selectivity, with the selectivity depending on some aspects of the current schedule. After a reward, when the monkeys knew that the upcoming cue would be valid, 88 of 246 (36%) neurons responded between schedules, seemingly anticipating the receiving information about the upcoming schedule length. When the cue appeared, 102 of 246 (41%) neurons became selective, at this point encoding information about whether the current trial was the only trial required or how many more trials are needed to obtain a reward. These cue-related responses had a median latency of 120 ms (just between the latencies in inferior temporal visual area TE and perirhinal cortex). When the monkey was releasing a touch bar to complete the trial correctly, 71 of 246 (29%) neurons responded, with responses in the rewarded trials being similar no matter which schedule was ending, thus being sensitive to the reward contingency. Finally, 39 of 246 (16%) neurons responded around the reward. We suggest that basolateral amygdala, by anticipating and then delineating the schedule and representing reward contingency, provide contextual information that is important for adjusting motivational level as a function of immediate behavior goals.

Short-term memory trace in rapidly adapting synapses of inferior temporal cortex.

Visual short-term memory tasks depend upon both the inferior temporal cortex (ITC) and the prefrontal cortex (PFC). Activity in some neurons persists after the first (sample) stimulus is shown. This delay-period activity has been proposed as an important mechanism for working memory. In ITC neurons, intervening (nonmatching) stimuli wipe out the delay-period activity; hence, the role of ITC in memory must depend upon a different mechanism. Here, we look for a possible mechanism by contrasting memory effects in two architectonically different parts of ITC: area TE and the perirhinal cortex. We found that a large proportion (80%) of stimulus-selective neurons in area TE of macaque ITCs exhibit a memory effect during the stimulus interval. During a sequential delayed matching-to-sample task (DMS), the noise in the neuronal response to the test image was correlated with the noise in the neuronal response to the sample image. Neurons in perirhinal cortex did not show this correlation. These results led us to hypothesize that area TE contributes to short-term memory by acting as a matched filter. When the sample image appears, each TE neuron captures a static copy of its inputs by rapidly adjusting its synaptic weights to match the strength of their individual inputs. Input signals from subsequent images are multiplied by those synaptic weights, thereby computing a measure of the correlation between the past and present inputs. The total activity in area TE is sufficient to quantify the similarity between the two images. This matched filter theory provides an explanation of what is remembered, where the trace is stored, and how comparison is done across time, all without requiring delay period activity. Simulations of a matched filter model match the experimental results, suggesting that area TE neurons store a synaptic memory trace during short-term visual memory.

Neuronal Mechanisms Encoding Global-to-Fine Information in Inferior-Temporal Cortex

Sugase et al. found that global information is represented at the initial transient firing of a single face-responsive neuron in inferior-temporal (IT) cortex, and that finer information is represented at the subsequent sustained firing. A feed-forward model and an attractor network are conceivable models to reproduce this dynamics. The attractor network, specifically an associative memory model, is employed to elucidate the neuronal mechanisms producing the dynamics. The results obtained by computer simulations show that a state of neuronal population initially approaches to a mean state of similar memory patterns, and that it finally converges to a memory pattern. This dynamics qualitatively coincides with that of face-responsive neurons. The dynamics of a single neuron in the model also coincides with that of a single face-responsive neuron. Furthermore, we propose two physiological experiments and predict the results from our model. Both predicted results are not explainable by the feed-forward model. Therefore, if the results obtained by actual physiological experiments coincide with our predicted results, the attractor network might be the neuronal mechanisms producing the dynamics of face-responsive neurons.

Stimulus-Related Activity during Conditional Associations in Monkey Perirhinal Cortex Neurons Depends on Upcoming Reward Outcome

Acquiring the significance of events based on reward-related information is critical for animals to survive and to conduct social activities. The importance of the perirhinal cortex for reward-related information processing has been suggested. To examine whether or not neurons in this cortex represent reward information flexibly when a visual stimulus indicates either a rewarded or unrewarded outcome, neuronal activity in the macaque perirhinal cortex was examined using a conditional-association cued-reward task. The task design allowed us to study how the neuronal responses depended on the animals prediction of whether it would or would not be rewarded. Two visual stimuli, a color stimulus as Cue1 followed by a pattern stimulus as Cue2, were sequentially presented. Each pattern stimulus was conditionally associated with both rewarded and unrewarded outcomes depending on the preceding color stimulus. We found an activity depending upon the two reward conditions during Cue2, i.e., pattern stimulus presentation. The response appeared after the response dependent upon the image identity of Cue2. The response delineating a specific cue sequence also appeared between the responses dependent upon the identity of Cue2 and reward conditions. Thus, when Cue1 sets the context for whether or not Cue2 indicates a reward, this region represents the meaning of Cue2, i.e., the reward conditions, independent of the identity of Cue2. These results suggest that neurons in the perirhinal cortex do more than associate a single stimulus with a reward to achieve flexible representations of reward information.

Face Inversion Decreased Information about Facial Identity and Expression in Face-Responsive Neurons in Macaque Area TE

To investigate the effect of face inversion and thatcherization (eye inversion) on temporal processing stages of facial information, single neuron activities in the temporal cortex (area TE) of two rhesus monkeys were recorded. Test stimuli were colored pictures of monkey faces (four with four different expressions), human faces (three with four different expressions), and geometric shapes. Modifications were made in each face-picture, and its four variations were used as stimuli: upright original, inverted original, upright thatcherized, and inverted thatcherized faces. A total of 119 neurons responded to at least one of the upright original facial stimuli. A majority of the neurons (71%) showed activity modulations depending on upright and inverted presentations, and a lesser number of neurons (13%) showed activity modulations depending on original and thatcherized face conditions. In the case of face inversion, information about the fine category (facial identity and expression) decreased, whereas information about the global category (monkey vs human vs shape) was retained for both the original and thatcherized faces. Principal component analysis on the neuronal population responses revealed that the global categorization occurred regardless of the face inversion and that the inverted faces were represented near the upright faces in the principal component analysis space. By contrast, the face inversion decreased the ability to represent human facial identity and monkey facial expression. Thus, the neuronal population represented inverted faces as faces but failed to represent the identity and expression of the inverted faces, indicating that the neuronal representation in area TE cause the perceptual effect of face inversion.

Differential Encoding of Factors Influencing Predicted Reward Value in Monkey Rostral Anterior Cingulate Cortex

Background The value of a predicted reward can be estimated based on the conjunction of both the intrinsic reward value and the length of time to obtain it. The question we addressed is how the two aspects, reward size and proximity to reward, influence the responses of neurons in rostral anterior cingulate cortex (rACC), a brain region thought to play an important role in reward processing. Methods and Findings We recorded from single neurons while two monkeys performed a multi-trial reward schedule task. The monkeys performed 1–4 sequential color discrimination trials to obtain a reward of 1–3 liquid drops. There were two task conditions, a valid cue condition, where the number of trials and reward amount were associated with visual cues, and a random cue condition, where the cue was picked from the cue set at random. In the valid cue condition, the neuronal firing is strongly modulated by the predicted reward proximity during the trials. Information about the predicted reward amount is almost absent at those times. In substantial subpopulations, the neuronal responses decreased or increased gradually through schedule progress to the predicted outcome. These two gradually modulating signals could be used to calculate the effect of time on the perception of reward value. In the random cue condition, little information about the reward proximity or reward amount is encoded during the course of the trial before reward delivery, but when the reward is actually delivered the responses reflect both the reward proximity and reward amount. Conclusions Our results suggest that the rACC neurons encode information about reward proximity and amount in a manner that is dependent on utility of reward information. The manner in which the information is represented could be used in the moment-to-moment calculation of the effect of time and amount on predicted outcome value.

Role of Temporal Processing Stages by Inferior Temporal Neurons in Facial Recognition

In this review, we focus on the role of temporal stages of encoded facial information in the visual system, which might enable the efficient determination of species, identity, and expression. Facial recognition is an important function of our brain and is known to be processed in the ventral visual pathway, where visual signals are processed through areas V1, V2, V4, and the inferior temporal (IT) cortex. In the IT cortex, neurons show selective responses to complex visual images such as faces, and at each stage along the pathway the stimulus selectivity of the neural responses becomes sharper, particularly in the later portion of the responses. In the IT cortex of the monkey, facial information is represented by different temporal stages of neural responses, as shown in our previous study: the initial transient response of face-responsive neurons represents information about global categories, i.e., human vs. monkey vs. simple shapes, whilst the later portion of these responses represents information about detailed facial categories, i.e., expression and/or identity. This suggests that the temporal stages of the neuronal firing pattern play an important role in the coding of visual stimuli, including faces. This type of coding may be a plausible mechanism underlying the temporal dynamics of recognition, including the process of detection/categorization followed by the identification of objects. Recent single-unit studies in monkeys have also provided evidence consistent with the important role of the temporal stages of encoded facial information. For example, view-invariant facial identity information is represented in the response at a later period within a region of face-selective neurons. Consistent with these findings, temporally modulated neural activity has also been observed in human studies. These results suggest a close correlation between the temporal processing stages of facial information by IT neurons and the temporal dynamics of face recognition.

Doubly sparse factor models for unifying feature transformation and feature selection

A number of unsupervised learning methods for high-dimensional data are largely divided into two groups based on their procedures, i.e., (1) feature selection, which discards irrelevant dimensions of the data, and (2) feature transformation, which constructs new variables by transforming and mixing over all dimensions. We propose a method that both selects and transforms features in a common Bayesian inference procedure. Our method imposes a doubly automatic relevance determination (ARD) prior on the factor loading matrix. We propose a variational Bayesian inference for our model and demonstrate the performance of our method on both synthetic and real data.

Small effect of upcoming reward outcomes on visual cue-related neuronal activity in macaque area TE during conditional associations

Area TE sends dense projections to the perirhinal cortex in macaque monkeys, an area in which we previously observed flexible signals regarding upcoming reward outcomes during a conditional-association cued-reward task. To investigate neuronal processing during the generation of information on upcoming reward outcomes, neuronal activities in area TE were examined. In the task, a color stimulus as Cue 1 and a pattern stimulus as Cue 2 were sequentially presented. Each pattern stimulus indicated both rewarded and unrewarded outcomes depending on the preceding color stimulus. In the activities during Cue 2 presentation, two-way analysis of variance revealed the effect of the interaction between Cue 1 and Cue 2, i.e., reward conditions, in 19 out of 133 neurons recorded in area TE. Of the 19 neurons, 12 also represented a response delineating a specific cue sequence, i.e., a trial-type activity. The latency of the reward-condition dependence in 7 neurons without the trial-type activity was indistinguishable from the latency in neurons without a trial-type activity in the perirhinal cortex. These results suggest that the effect of upcoming reward conditions is small in area TE and that the representation of reward conditions arises in areas beyond the ventral visual pathway, including the perirhinal cortex, during conditional associations.

Information Accumulation over Time in Monkey Inferior Temporal Cortex Neurons Explains Pattern Recognition Reaction Time under Visual Noise

We recognize objects even when they are partially degraded by visual noise. We studied the relation between the amount of visual noise (5, 10, 15, 20, or 25%) degrading 8 black-and-white stimuli and stimulus identification in 2 monkeys performing a sequential delayed match-to-sample task. We measured the accuracy and speed with which matching stimuli were identified. The performance decreased slightly (errors increased) as the amount of visual noise increased for both monkeys. The performance remained above 80% correct, even with 25% noise. However, the reaction times markedly increased as the noise increased, indicating that the monkeys took progressively longer to decide what the correct response would be as the amount of visual noise increased, showing that the monkeys trade time to maintain accuracy. Thus, as time unfolds the monkeys act as if they are accumulating the information and/or testing hypotheses about whether the test stimulus is likely to be a match for the sample being held in short-term memory. We recorded responses from 13 single neurons in area TE of the 2 monkeys. We found that stimulus-selective information in the neuronal responses began accumulating when the match stimulus appeared. We found that the greater the amount of noise obscuring the test stimulus, the more slowly stimulus-related information by the 13 neurons accumulated. The noise induced slowing was about the same for both behavior and information. These data are consistent with the hypothesis that area TE neuron population carries information about stimulus identity that accumulates over time in such a manner that it progressively overcomes the signal degradation imposed by adding visual noise.