[Show abstract][Hide abstract] ABSTRACT: 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.
Journal of Neuroscience 07/2014; 34(28):9377-88. · 6.75 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: 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.
Brain research 11/2011; 1423:30-40. · 2.83 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Precise localization of single-neuron activity has elucidated functional architectures of the primate cerebral cortex, related to vertically stacked layers and horizontally aligned columns. The traditional "gold standard" method for localizing recorded neuron is histological examination of electrolytic lesion marks at recording sites. Although this method can localize recorded neurons with fine neuroanatomy, the necessity for postmortem analysis prohibits its use in long-term chronic experiments. To localize recorded single-neuron positions in vivo, we introduced MRI-detectable elgiloy deposit marks, which can be created by electrolysis of an elgiloy microelectrode tip and visualized on highly contrasted magnetic resonance (MR) images. Histological analysis validated that the deposit mark centers could be localized relative to neuroanatomy in vivo with single-voxel accuracy, at an in-plane resolution of 200 μm. To demonstrate practical applications of the technique, we recorded single-neuron activity from a monkey performing a cognitive task and localized it in vivo using deposit marks (deposition: 2 μA for 3 min; scanning: fast-spin-echo sequence with 0.15 × 0.15 × 0.8 mm(3) resolution, 120/4,500 ms of echo-time/repetition-time and 8 echo-train-length), as is usually performed with conventional postmortem methods using electrolytic lesion marks. Two localization procedures were demonstrated: 1) deposit marks within a microelectrode track were used to reconstruct a dozen recorded neuron positions along the track directly on MR images; 2) combination with X-ray imaging allowed estimation of hundreds of neuron positions on MR images. This new in vivo method is feasible for chronic experiments with nonhuman primates, enabling analysis of the functional architecture of the cerebral cortex underlying cognitive processes.
Journal of Neurophysiology 12/2010; 105(3):1380-92. · 3.04 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The perirhinal cortex, which is critical for long-term stimulus-stimulus associative memory, consists of two cytoarchitectonically distinct subdivisions: area 35 (A35) and area 36 (A36). Previous electrophysiological studies suggested that macaque A36 is involved in both association and retrieval processes during a visual pair-association task. However, the neuronal properties of macaque A35 have never been examined because A35 is located in a very narrow region, which makes it difficult to systematically record single-unit activity from there. In the present study, we overcame this technical difficulty for targeting A35 by combining magnetic resonance imaging-guided in-vivo localization with postmortem histological localization. This two-track approach enabled us to record from 181 A35 neurons in two macaque monkeys while they performed a pair-association task. Among these neurons, 64 showed stimulus-selective responses during the cue period (cue-selective neurons), whereas 18 did during the delay period (delay-selective neurons). As in A36, the responses of cue-selective neurons in A35 to paired associates were correlated. In both areas, these correlations were stronger in neurons showing delay selectivity than in those without delay selectivity. Notably, delay-selective neurons in A35 responded similarly to the optimal stimulus and its paired associate, whereas delay-selective neurons in A36 discriminated between them. However, these neurons in both areas discriminated the primary pair, consisting of the optimal stimulus and its paired associate, from other pairs, indicating that selectivity across pairs was maintained between the two areas. These results suggest that delay-selective neurons in A35 represent these paired stimuli as a single unitized item rather than two associated items.
European Journal of Neuroscience 08/2010; 32(4):659-67. · 3.67 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The localization of microelectrode recording sites in the layers of primate cerebral cortex permits the analysis of relationships between recorded neuronal activities and underlying anatomical connections. We present a magnetic resonance imaging method for precise in vivo localization of cortical recording sites. In this method, the susceptibility-induced effect thickens the appearance of the microelectrode and enhances the detectability of the microelectrode tip, which usually occupies less than a few percent of the volume of an image voxel. In a phantom study, the optimized susceptibility-induced effect allowed tip detection with single-voxel accuracy (in-plane resolution, 50 mum). We applied this method to recording microelectrodes inserted into the brains of macaque monkeys, and localized the microelectrode tip at an in-plane resolution of 150 mum within the cortex of 2-3 mm in thickness. Subsequent histological analyses validated the single-voxel accuracy of the in vivo tip localization. This method opens up a way to investigate information flow during cognitive processes in the brain.
[Show abstract][Hide abstract] ABSTRACT: We investigated the contribution of the inferior temporal (IT) cortical neurons to the active maintenance of internal representations. The activity of single neurons in the IT cortex was recorded while the monkeys performed a sequential-type associative memory task in which distractor stimuli interrupted the delay epoch between the cue and target (paired-associate) stimuli. For each neuron, information about each stimulus conveyed by the delay activity was estimated as a coefficient of multiple regression analysis. We found that target information derived from long-term memory (LTM) persisted despite the distractors. By contrast, cue information derived from the visual system was attenuated and frequently replaced by distractor information. These results suggest that LTM-derived information required for upcoming behavior is actively maintained in the IT neurons, whereas visually derived information tends to be updated irrespective of behavioral relevance.
[Show abstract][Hide abstract] ABSTRACT: The macaque inferotemporal cortex, which is involved in encoding and retrieval of visual long-term memory, consists of two distinct but mutually interconnected areas: area TE (TE) and area 36 (A36). In the present study, we compared delay-period activities of the two subdivisions in terms of their signal contents. We recorded single-unit activities from TE and A36 during a delayed pair association task, in which monkeys were required to choose the paired associate of a cue stimulus after a delay period. The stimulus-selective delay-period activities of single neurons were characterized by using partial correlation coefficients of delay-period activities for each cue stimulus with the cue-period responses to that stimulus (cue-holding index, CHI) and with the cue-period responses to its paired associate (pair-recall index, PRI). The delay-period activities of TE neurons preferentially represented the paired associate (PRI, median = 0.54) rather than the cue stimulus itself (CHI, 0.23) (P < 0.001, n = 70), while the delay-period activities of A36 neurons retained both the cue stimulus and its paired associate equivalently (CHI, 0.44; PRI, 0.46) (P = 0.78, n = 38). These results indicate that the signal contents of delay-period activities differ between the two subdivisions: TE mostly represents a sought target that is retrieved from long-term memory, while A36 in addition retains cue-stimulus that is transmitted from earlier visual areas.
European Journal of Neuroscience 11/2003; 18(10):2915-8. · 3.67 Impact Factor