Toshiyuki Hirabayashi

Reversal of Interlaminar Signal Between Sensory and Memory Processing in Monkey Temporal Cortex

Feed-forward signals flowing across cortical layers during sensory coding reverse direction during memory retrieval. The primate temporal cortex implements visual long-term memory. However, how its interlaminar circuitry executes cognitive computations is poorly understood. Using linear-array multicontact electrodes, we simultaneously recorded unit activities across cortical layers in the perirhinal cortex of macaques performing a pair-association memory task. Cortical layers were estimated on the basis of current source density profiles with histological verifications, and the interlaminar signal flow was determined with cross-correlation analysis between spike trains. During the cue period, canonical “feed-forward” signals flowed from granular to supragranular layers and from supragranular to infragranular layers. During the delay period, however, the signal flow reversed to the “feed-back” direction: from infragranular to supragranular layers. This reversal of signal flow highlights how the temporal cortex differentially recruits its laminar circuits for sensory and mnemonic processing.

Dynamically Modulated Spike Correlation in Monkey Inferior Temporal Cortex Depending on the Feature Configuration within a Whole Object

The mechanism underlying the processing of spatially separated multiple local features to form a unique whole object is an important issue in visual object recognition. We tested whether, in behaving monkeys, the spike correlation between pairs of inferior temporal (IT) neurons dynamically changes depending on the spatial configuration of the local features within a whole object. We prepared more than 60,000 face-like objects (FOs) and their corresponding non-face-like objects (NFOs) that consisted of random arrangements of the same set of local features as those in FOs. The spike correlation between a pair of neurons was quantified by the peak height of the shift predictor-subtracted cross-correlogram. For both neurons of the pair, the local features in a whole object were determined so that they elicited as high a response as possible to enable a reliable cross-correlation analysis. We found that the FOs thus constructed elicited neuronal activities that were more strongly correlated than the corresponding NFOs. Firing rates of the same neurons did not show such a consistent bias depending on the feature configuration. Furthermore, receiver operating characteristic analysis revealed that this FO dominance of spike correlation was robust enough to discriminate between different feature configurations at the population level. Spike correlation of the cell pairs exhibited significant FO dominance within 300 ms after stimulus onset. The present results suggest that feature configuration within a unique whole object can be reflected in the rapid modulation of spike correlation among a population of neurons in the IT cortex.

Microcircuits for hierarchical elaboration of object coding across primate temporal areas.

Hierarchy and Representation Neuronal representations of objects are elaborated through the hierarchy of occipitotemporal cortical areas, and the recognition of a feature as “novel” is commonly thought to emerge and become prevalent at a cortical area because of local signal processing. Hirabayashi et al. (p. 191) tested another possibility—that a feature representation becomes prevalent in a given area because a microcircuit creates a small number of precursor representations in a prior area in the cortical hierarchy, and the representations then become prevalent through proliferation in the subsequent area. In support of this notion, critical microcircuits for object association were observed using multiple single-unit recordings in two areas of the macaque temporal cortex. Neuronal activity representing novel features emerges in hierarchically lower brain areas earlier than previously thought. In primates, neuronal representations of objects are processed hierarchically in occipitotemporal cortices. A “novel” feature of objects is thought to emerge and become prevalent at a cortical area because of processing in this area. We tested the possibility that a feature representation prevalent in a given area emerges in the microcircuit of a hierarchically prior area as a small number of prototypes and then becomes prevalent in the subsequent area. We recorded multiple single units in each of hierarchically sequential areas TE and 36 of macaque temporal cortex and found the predicted convergent microcircuit for object-object association in area TE. Associative codes were then built up over time in the microcircuit of area 36. These results suggest a computational principle underlying sequentially elaborated object representations.

Triphasic Dynamics of Stimulus-Dependent Information Flow between Single Neurons in Macaque Inferior Temporal Cortex

The functional connectivity between cortical neurons is not static and is known to exhibit contextual modulations in terms of the coupling strength. Here we hypothesized that the information flow in a cortical local circuit exhibits complex forward-and-back dynamics, and conducted Granger causality analysis between the neuronal spike trains that were simultaneously recorded from macaque inferior temporal (IT) cortex while the animals performed a visual object discrimination task. Spikes from neuron pairs with a displaced peak on the cross-correlogram (CCG) showed Granger causality in the gamma-frequency range (30–80 Hz) with the dominance in the direction consistent with the CCG peak (forward direction). Although, in a classical view, the displaced CCG peak has been interpreted as an indicative of a pauci-synaptic serial linkage, temporal dynamics of the gamma Granger causality after stimulus onset exhibited a more complex triphasic pattern, with a transient forward component followed by a slowly developing backward component and subsequent reappearance of the forward component. These triphasic dynamics of causality were not explained by the firing rate dynamics and were not observed for cell pairs that exhibited a center peak on the CCG. Furthermore, temporal dynamics of Granger causality depended on the feature configuration within the presented object. Together, these results demonstrate that the classical view of functional connectivity could be expanded to incorporate more complex forward-and-back dynamics and also imply that multistage processing in the recognition of visual objects might be implemented by multiphasic dynamics of directional information flow between single neurons in a local circuit in the IT cortex.

Top-Down Regulation of Laminar Circuit via Inter-Area Signal for Successful Object Memory Recall in Monkey Temporal Cortex.

Memory retrieval in primates is orchestrated by a brain-wide neuronal circuit. To elucidate the operation of this circuit, it is imperative to comprehend neuronal mechanisms of coordination between area-to-area interaction and information processing within individual areas. By simultaneous recording from area 36 (A36) and area TE (TE) of the temporal cortex while monkeys performed a pair-association memory task, we found two distinct inter-area signal flows during memory retrieval: A36 spiking activity exhibited coherence with low-frequency field activity in either the supragranular or infragranular layer of TE. Of these two flows, only signal flow targeting the infragranular layer of TE was further translaminarly coupled with gamma activity in the supragranular layer of TE. Moreover, this coupling was observed when monkeys succeeded in the retrieval of the sought object but not when they failed. The results suggest that local translaminar processing can be recruited via a layer-specific inter-area network for memory retrieval.

Computational principles of microcircuits for visual object processing in the macaque temporal cortex

Understanding the principles of neuronal computation that underlie our cognitive abilities is a fundamental goal of neuroscience. Microcircuits are thought to be computational units embedded in a brain-wide neuronal network. Recent progress in experimental and analytical techniques has enabled the exploration of information flow in operating microcircuits of behaving monkeys. Accumulating evidence demonstrates that crucial transformations of neuronal codes for the representation and memory retrieval of visual objects occur in cortical microcircuits. Particularly, microcircuit comparisons across cortical areas provide novel principles for object processing, in which precursor codes for object features are constructed in a lower-order area before prevalence in a higher-order area. We review recent findings on microcircuit operations in macaque temporal cortex that enable object processing, and discuss future research directions.

Distinct Neuronal Interactions in Anterior Inferotemporal Areas of Macaque Monkeys during Retrieval of Object Association Memory

In macaque monkeys, the anterior inferotemporal cortex, a region crucial for object memory processing, is composed of two adjacent, hierarchically distinct areas, TE and 36, for which different functional roles and neuronal responses in object memory tasks have been characterized. However, it remains unknown how the neuronal interactions differ between these areas during memory retrieval. Here, we conducted simultaneous recordings from multiple single-units in each of these areas while monkeys performed an object association memory task and examined the inter-area differences in neuronal interactions during the delay period. Although memory neurons showing sustained activity for the presented cue stimulus, cue-holding (CH) neurons, interacted with each other in both areas, only those neurons in area 36 interacted with another type of memory neurons coding for the to-be-recalled paired associate (pair-recall neurons) during memory retrieval. Furthermore, pairs of CH neurons in area TE showed functional coupling in response to each individual object during memory retention, whereas the same class of neuron pairs in area 36 exhibited a comparable strength of coupling in response to both associated objects. These results suggest predominant neuronal interactions in area 36 during the mnemonic processing, which may underlie the pivotal role of this brain area in both storage and retrieval of object association memory.

Conversion of object identity to object-general semantic value in the primate temporal cortex

Faulty remembrance of objects past The primate brain analyzes visual input along the ventral processing stream to extract the identity of an object. The final stage of this stream, the perirhinal cortex, plays a crucial role in object recognition. Tamura et al. systematically biased the judgments of monkeys in an old-new object recognition task by using either optogenetic or electrical stimulation. The monkeys judged an encountered object as familiar when the stimulation site was in a hotspot where memory neurons were clustered. However, at the hotspots fringe region, where neurons lost selective responses to the learned objects, electrical microstimulation led the monkeys to mistakenly judge an object as never seen before. Science, this issue p. 687 Optogenetic activation of perirhinal memory neurons in primates drives a subjective feeling of having previously seen an object. At the final stage of the ventral visual stream, perirhinal neurons encode the identity of memorized objects through learning. However, it remains elusive whether and how object percepts alone, or concomitantly a nonphysical attribute of the objects (“learned”), are decoded from perirhinal activities. By combining monkey psychophysics with optogenetic and electrical stimulations, we found a focal spot of memory neurons where both stimulations led monkeys to preferentially judge presented objects as “already seen.” In an adjacent fringe area, where neurons did not exhibit selective responses to the learned objects, electrical stimulation induced the opposite behavioral bias toward “never seen before,” whereas optogenetic stimulation still induced bias toward “already seen.” These results suggest that mnemonic judgment of objects emerges via the decoding of their nonphysical attributes encoded by perirhinal neurons.

Submodality-dependent spatial organization of neurons coding for visual long-term memory in macaque inferior temporal cortex

The inferior temporal (IT) cortex has been shown to serve as a storehouse of visual long-term memory for object shapes. However, it is currently unclear how information regarding multiple visual attributes of objects, including shape and color, is stored and retrieved in an organized way. Specifically, the question of whether information regarding different visual attributes is encoded by different neurons, and the spatial organization of neurons that encode visual attribute-dependent object information remain to be elucidated. In the present study, we trained monkeys to perform a pair-association task with two stimulus sets, in which individual stimuli were either visually discernible by shape or by color. We examined both the responses of single neurons and their spatial distributions in area 36 of the IT cortex. We found that a significant majority of visually responsive neurons showed stimulus selectivity for only one of the two visual attributes. Moreover, neuronal activity encoding the learned pair-associations was observed only in neurons that exhibited stimulus selectivity for one of the two visual attributes. A spatial distribution analysis demonstrated that the neurons coding for each stimulus set were not randomly distributed, but were localized in two separate clusters, each corresponding to a different visual attribute. Together, these results suggest that pair-association memory for different visual attributes is distinctly stored in the IT cortex both in terms of neuronal responses and the spatial organization of neurons coding for each visual attribute.

Sensory and mnemonic demands flexibly recruit interlaminar microcircuits in macaque temporal cortex

orientation map obtained by OISI. As a result, fOCT revealed that optimal orientation was roughly the same along the depth axis, and the orientation shifted gradually along the axis parallel to the cortical surface consistent with the classical view of columnar organization. Integrated orientation selectivity from depth showed high correlation with OISI result (R > 0.7). However, sudden change in optimal orientation selectivity was also observed locally in depth axis unlike previous studies.