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The ability to infer others' mental states is essential to social interactions. This ability, critically evaluated by testing whether one attributes false beliefs (FBs) to others, has been considered to be uniquely hominid and to accompany the activation of a distributed brain network. We challenge the taxon specificity of this ability and identify the causal brain locus by introducing an anticipatory-looking FB paradigm combined with chemogenetic neuronal manipulation in macaque monkeys. We find spontaneous gaze bias of macaques implicitly anticipating others' FB-driven actions. Silencing of the medial prefrontal neuronal activity with inhibitory designer receptor exclusively activated by designer drugs (DREADDs) specifically eliminates the implicit gaze bias while leaving the animals' visually guided and memory-guided tracking abilities intact. Thus, neuronal activity in the medial prefrontal cortex could have a causal role in FB-attribution-like behaviors in the primate lineage, emphasizing the importance of probing the neuronal mechanisms underlying theory of mind with relevant macaque animal models.

DOI： 10.1016/j.celrep.2020.03.013

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Language：Japanese   Publisher：(一社)日本生理学会  

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Language：Japanese   Publisher：(一社)日本生理学会  

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Language：Japanese   Publisher：(一社)日本生理学会  

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Language：Japanese   Publisher：(公社)日本精神神経学会  

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DOI： 10.1109/BIBM47256.2019.8983029

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Other Link： https://dblp.uni-trier.de/db/conf/bibm/bibm2019.html#DateKHO19

Language：English   Publishing type：Research paper (scientific journal)   Publisher：Nature Publishing Group  

Propagation of oscillatory spike firing activity at specific frequencies plays an important role in distributed cortical networks. However, there is limited evidence for how such frequency-specific signals are induced or how the signal spectra of the propagating signals are modulated during across-layer (radial) and inter-areal (tangential) neuronal interactions. To directly evaluate the direction specificity of spectral changes in a spiking cortical network, we selectively photostimulated infragranular excitatory neurons in the rat primary visual cortex (V1) at a supra-threshold level with various frequencies, and recorded local field potentials (LFPs) at the infragranular stimulation site, the cortical surface site immediately above the stimulation site in V1, and cortical surface sites outside V1. We found a significant reduction of LFP powers during radial propagation, especially at high-frequency stimulation conditions. Moreover, low-gamma-band dominant rhythms were transiently induced during radial propagation. Contrastingly, inter-areal LFP propagation, directed to specific cortical sites, accompanied no significant signal reduction nor gamma-band power induction. We propose an anisotropic mechanism for signal processing in the spiking cortical network, in which the neuronal rhythms are locally induced/modulated along the radial direction, and then propagate without distortion via intrinsic horizontal connections for spatiotemporally precise, inter-areal communication.

DOI： 10.1038/s41598-018-26054-8

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The inferior temporal cortex (ITC) contains neurons selective to multiple levels of visual categories. However, the mechanisms by which these neurons collectively construct hierarchical category percepts remain unclear. By comparing decoding accuracy with simultaneously acquired electrocorticogram (ECoG), local field potentials (LFPs), and multi-unit activity in the macaque ITC, we show that low-frequency LFPs/ECoG in the early evoked visual response phase contain sufficient coarse category (e.g., face) information, which is homogeneous and enhanced by spatial summation of up to several millimeters. Late-induced high-frequency LFPs additionally carry spike-coupled finer category (e.g., species, view, and identity of the face) information, which is heterogeneous and reduced by spatial summation. Face-encoding neural activity forms a cluster in similar cortical locations regardless of whether it is defined by early evoked low-frequency signals or late-induced high-gamma signals. By contrast, facial subcategory-encoding activity is distributed, not confined to the face cluster, and dynamically increases its heterogeneity from the early evoked to late-induced phases. These findings support a view that, in contrast to the homogeneous and static coarse category-encoding neural cluster, finer category-encoding clusters are heterogeneously distributed even outside their parent category cluster and dynamically increase heterogeneity along with the local cortical processing in the ITC.

DOI： 10.1093/cercor/bhx342

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：NATURE PUBLISHING GROUP  

Highly localized neuronal spikes in primate temporal cortex can encode associative memory; however, whether memory formation involves area-wide reorganization of ensemble activity, which often accompanies rhythmicity, or just local microcircuit-level plasticity, remains elusive. Using high-density electrocorticography, we capture local-field potentials spanning the monkey temporal lobes, and show that the visual pair-association (PA) memory is encoded in spatial patterns of theta activity in areas TE, 36, and, partially, in the parahippocampal cortex, but not in the entorhinal cortex. The theta patterns elicited by learned paired associates are distinct between pairs, but similar within pairs. This pattern similarity, emerging through novel PA learning, allows a machine-learning decoder trained on theta patterns elicited by a particular visual item to correctly predict the identity of those elicited by its paired associate. Our results suggest that the formation and sharing of widespread cortical theta patterns via learning-induced reorganization are involved in the mechanisms of associative memory representation.

DOI： 10.1038/ncomms11827

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Language：Japanese   Publisher：Japanese Society for Medical and Biological Engineering  

<p>Converging evidence suggests that cortical processing is performed in a hierarchical manner. In the primate object vision, visual information is thought to be processed along the sequence of areas. We identified the direct physiological evidence for the cortical hierarchical processing as propagating activity patterns by employing electrocorticography (ECoG) in monkey, which enable us to record neural activity from wide cortical areas at high spatiotemporal resolution. Quantification of the propagating wave by symbolic local transfer entropy (SLTE) revealed both feed-forward and feedback components. We also found that SLTE topography changed during the visual stimulation. We also examined hierarchal nature of the process by comparing the ECoG activity pattern with the output from each layer of a deep neural network model. The output explained the specific spatiotemporal aspect of the ECoG activity. These results add the physiological insights of the hierarchical processing in the ventral visual stream.</p>

DOI： 10.11239/jsmbe.54Annual.S291

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS INC  

Recognition of faces and written words is associated with category-specific brain activation in the ventral occipitotemporal cortex (vOT). However, topological and functional relationships between face-selective and word-selective vOT regions remain unclear. In this study, we collected data from patients with intractable epilepsy who underwent high-density recording of surface field potentials in the vOT. "Faces" and "letterstrings" induced outstanding category-selective responses among the 24 visual categories tested, particularly in high-gamma band powers. Strikingly, within-hemispheric analysis revealed alternation of face-selective and letterstring-selective zones within the vOT. Two distinct face-selective zones located anterior and posterior portions of the mid-fusiform sulcus whereas letterstring-selective zones alternated between and outside of these 2 face-selective zones. Further, a classification analysis indicated that activity patterns of these zones mostly represent dedicated categories. Functional connectivity analysis using Granger causality indicated asymmetrically directed causal influences from face-selective to letterstring-selective regions. These results challenge the prevailing view that different categories are represented in distinct contiguous regions in the vOT.

DOI： 10.1093/cercor/bht319

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：ACADEMIC PRESS INC ELSEVIER SCIENCE  

How visual object categories are represented in the brain is one of the key questions in neuroscience. Studies on low-level visual features have shown that relative timings or phases of neural activity between multiple brain locations encode information. However, whether such temporal patterns of neural activity are used in the representation of visual objects is unknown. Here, we examined whether and how visual object categories could be predicted (or decoded) from temporal patterns of electrocorticographic (ECoG) signals from the temporal cortex in five patients with epilepsy. We used temporal correlations between electrodes as input features, and compared the decoding performance with features defined by spectral power and phase from individual electrodes. While using power or phase alone, the decoding accuracy was significantly better than chance, correlations alone or those combined with power outperformed other features. Decoding performance with correlations was degraded by shuffling the order of trials of the same category in each electrode, indicating that the relative time series between electrodes in each trial is critical. Analysis using a sliding time window revealed that decoding performance with correlations began to rise earlier than that with power. This earlier increase in performance was replicated by a model using phase differences to encode categories. These results suggest that activity patterns arising from interactions between multiple neuronal units carry additional information on visual object categories. (C) 2013 The Authors. Published by Elsevier Inc. All rights reserved.

DOI： 10.1016/j.neuroimage.2013.12.020

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Language：English   Publishing type：Research paper (international conference proceedings)   Publisher：IEEE  

In order to realize a low-invasive and high accuracy Brain-Machine Interface (BMI) system for clinical applications, a super multi-channel recording system was developed in which 4096 channels of Electrocorticogram (ECoG) signal can be amplified and transmitted to outside the body by using an Ultra Wide Band (UWB) wireless system. Also, a high density, flexible electrode array made by using a Parylene-C substrate was developed that is composed of units of 32-ch recording arrays. We have succeeded in an evaluation test of UWB wireless transmitting using a body phantom system.

DOI： 10.1109/EMBC.2014.6944799

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：LIPPINCOTT WILLIAMS & WILKINS  

BACKGROUND: There has been growing interest in clinical single-neuron recording to better understand epileptogenicity and brain function. It is crucial to compare this new information, single-neuronal activity, with that obtained from conventional intracranial electroencephalography during simultaneous recording. However, it is difficult to implant microwires and subdural electrodes during a single surgical operation because the stereotactic frame hampers flexible craniotomy.
OBJECTIVE: To describe newly designed electrodes and surgical techniques for implanting them with subdural electrodes that enable simultaneous recording from hippocampal neurons and broad areas of the cortical surface.
METHODS: We designed a depth electrode that does not protrude into the dura and pulsates naturally with the brain. The length and tract of the depth electrode were determined preoperatively between the lateral subiculum and the lateral surface of the temporal lobe. A frameless navigation system was used to insert the depth electrode. Surface grids and ventral strips were placed before and after the insertion of the depth electrodes, respectively. Finally, a microwire bundle was inserted into the lumen of the depth electrode. We evaluated the precision of implantation, the recording stability, and the recording rate with microwire electrodes.
RESULTS: Depth-microwire electrodes were placed with a precision of 3.6 mm. The mean successful recording rate of single-or multiple-unit activity was 14.8%, which was maintained throughout the entire recording period.
CONCLUSION: We achieved simultaneous implantation of microwires, depth electrodes, and broad-area subdural electrodes. Our method enabled simultaneous and stable recording of hippocampal single-neuron activities and multichannel intracranial electroencephalography.

DOI： 10.1227/01.neu.0000430327.48387.e1

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Language：English   Publisher：Japanese Society for Medical and Biological Engineering  

DOI： 10.11239/jsmbe.51.M-2

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：PERGAMON-ELSEVIER SCIENCE LTD  

Viral vector-mediated gene transfer has become increasingly valuable for primate brain research, in particular for application of genetic methods (e.g. optogenetics) to study neuronal circuit functions. Neuronal cell tropisms and infection patterns are viable options for obtaining viral vector-mediated transgene delivery that is selective for particular neuronal pathways. For example, several types of viral vectors can infect axon terminals (retrograde infections), which enables targeted transgene delivery to neurons that directly project to a particular viral injection region. Although recent studies in rodents have demonstrated that adeno-associated virus serotype 8 (AAV8) and 9 (AAV9) efficiently transduce neurons, the tropisms and infection patterns remain poorly understood in primate brains. Here, we constructed recombinant AAV8 or AAV9, which expressed an enhanced green fluorescent protein (EGFP) gene driven by a ubiquitous promoter (AAV8-EGFP and AAV9-EGFP, respectively), and stereotaxically injected it into several brain regions in marmosets and macaque monkeys. Immunohistochemical analyses revealed almost exclusive colocalization of EGFP fluorescence via AAV9-mediated gene transfer with a neuron-specific marker, indicating endogenous neuronal tropism of AAV9, which was consistent with our previous results utilizing AAV8. Injections of either AAV8-EGFP or AAV9-EGFP into the marmoset striatum resulted in EGFP expression in local striatal neurons as a result of local infection, as well as expression in dopaminergic neurons of the substantia nigra via retrograde transport along nigrostriatal axonal projections. Retrograde infections were also observed in the frontal cortex and thalamus, which are known to have direct projections to the striatum. These local and retrograde gene transfers were further demonstrated in the geniculocortical pathway of the marmoset visual system. These findings indicate promising capabilities of AAV8 and AAV9 to deliver molecular tools into a range of primate neural systems in pathway-specific manners through their neuronal tropisms and infection patterns. (C) 2011 IBRO. Published by Elsevier Ltd. All rights reserved.

DOI： 10.1016/j.neuroscience.2011.06.080

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：PERGAMON-ELSEVIER SCIENCE LTD  

Viral vector-mediated gene transfer has become increasingly valuable for primate brain research, in particular for application of genetic methods (e.g. optogenetics) to study neuronal circuit functions. Neuronal cell tropisms and infection patterns are viable options for obtaining viral vector-mediated transgene delivery that is selective for particular neuronal pathways. For example, several types of viral vectors can infect axon terminals (retrograde infections), which enables targeted transgene delivery to neurons that directly project to a particular viral injection region. Although recent studies in rodents have demonstrated that adeno-associated virus serotype 8 (AAV8) and 9 (AAV9) efficiently transduce neurons, the tropisms and infection patterns remain poorly understood in primate brains. Here, we constructed recombinant AAV8 or AAV9, which expressed an enhanced green fluorescent protein (EGFP) gene driven by a ubiquitous promoter (AAV8-EGFP and AAV9-EGFP, respectively), and stereotaxically injected it into several brain regions in marmosets and macaque monkeys. Immunohistochemical analyses revealed almost exclusive colocalization of EGFP fluorescence via AAV9-mediated gene transfer with a neuron-specific marker, indicating endogenous neuronal tropism of AAV9, which was consistent with our previous results utilizing AAV8. Injections of either AAV8-EGFP or AAV9-EGFP into the marmoset striatum resulted in EGFP expression in local striatal neurons as a result of local infection, as well as expression in dopaminergic neurons of the substantia nigra via retrograde transport along nigrostriatal axonal projections. Retrograde infections were also observed in the frontal cortex and thalamus, which are known to have direct projections to the striatum. These local and retrograde gene transfers were further demonstrated in the geniculocortical pathway of the marmoset visual system. These findings indicate promising capabilities of AAV8 and AAV9 to deliver molecular tools into a range of primate neural systems in pathway-specific manners through their neuronal tropisms and infection patterns. (C) 2011 IBRO. Published by Elsevier Ltd. All rights reserved.

DOI： 10.1016/j.neuroscience.2011.06.080

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Language：English   Publishing type：Research paper (scientific journal)  

Electrocorticography (ECoG), multichannel brain-surface recording and stimulation with probe electrode arrays, has become a potent methodology not only for clinical neurosurgery but also for basic neuroscience using animal models. The highly evolved primate's brain has deep cerebral sulci, and both gyral and intrasulcal cortical regions have been implicated in important functional processes. However, direct experimental access is typically limited to gyral regions, since placing probes into sulci is difficult without damaging the surrounding tissues. Here we describe a novel methodology for intrasulcal ECoG in macaque monkeys. We designed and fabricated ultra-thin flexible probes for macaques with micro-electro-mechanical systems (MEMS) technology. We developed minimally invasive operative protocols to implant the probes by introducing cutting edge devices for human neurosurgery. To evaluate the feasibility of intrasulcal ECoG, we conducted electrophysiological recording and stimulation experiments. First, we inserted parts of the Parylene-C-based probe into the superior temporal sulcus to compare visually evoked ECoG responses from the ventral bank of the sulcus with those from the surface of the inferior temporal cortex. Analyses of power spectral density and signal-to-noise ratio revealed that the quality of the ECoG signal was comparable inside and outside of the sulcus. Histological examination revealed no obvious physical damage in the implanted areas. Second, we placed a modified silicone ECoG probe into the central sulcus and also on the surface of the precentral gyrus for stimulation. Thresholds for muscle twitching were significantly lower during intrasulcal stimulation compared to gyral stimulation. These results demonstrate the feasibility of intrasulcal ECoG in macaques. The novel methodology proposed here opens up a new frontier in neuroscience research, enabling the direct measurement and manipulation of electrical activity in the whole brain. © 2011 Matsuo, Kawasaki, Osada, Sawahata, Suzuki, Shibata, Miyakawa, Nakahara, Iijima, Sato, Kawai, Saito and Hasegawa.

DOI： 10.3389/fnsys.2011.00034

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DOI： 10.1016/j.neures.2011.07.415

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DOI： 10.1016/j.neures.2011.07.1812

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS INC  

Long-term familiarity facilitates recognition of visual stimuli. To better understand the neural basis for this effect, we measured the local field potential (LFP) and multiunit spiking activity (MUA) from the inferior temporal (IT) lobe of behaving monkeys in response to novel and familiar images. In general, familiar images evoked larger amplitude LFPs whereas MUA responses were greater for novel images. Familiarity effects were attenuated by image rotations in the picture plane of 45 degrees. Decreasing image contrast led to more pronounced decreases in LFP response magnitude for novel, compared with familiar images, and resulted in more selective MUA response profiles for familiar images. The shape of individual LFP traces could be used for stimulus classification, and classification performance was better for the familiar image category. Recording the visual and auditory evoked LFP at multiple depths showed significant alterations in LFP morphology with distance changes of 2 mm. In summary, IT cortex shows local processing differences for familiar and novel images at a time scale and in a manner consistent with the observed behavioral advantage for classifying familiar images and rapidly detecting novel stimuli.

DOI： 10.1093/cercor/bhn015

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：AMER PHYSIOLOGICAL SOC  

The malleability of object representations by experience is essential for adaptive behavior. It has been hypothesized that neurons in inferior temporal cortex (IT) in monkeys are pivotal in visual association learning, evidenced by experiments revealing changes in neural selectivity following visual learning, as well as by lesion studies, wherein functional inactivation of IT impairs learning. A critical question remaining to be answered is whether IT neuronal activity is sufficient for learning. To address this question directly, we conducted experiments combining visual classification learning with microstimulation in IT. We assessed the effects of IT microstimulation during learning in cases where the stimulation was exclusively informative, conditionally informative, and informative but not necessary for the classification task. The results show that localized microstimulation in IT can be used to establish visual classification learning, and the same stimulation applied during learning can predictably bias judgments on subsequent recognition. The effect of induced activity can be explained neither by direct stimulation- motor association nor by simple detection of cortical stimulation. We also found that the learning effects are specific to IT stimulation as they are not observed by microstimulation in an adjacent auditory area. Our results add the evidence that the differential activity in IT during visual association learning is sufficient for establishing new associations. The results suggest that experimentally manipulated activity patterns within IT can be effectively combined with ongoing visually induced activity during the formation of new associations.

DOI： 10.1152/jn.90247.2008

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：OXFORD UNIV PRESS INC  

Although some change in the neural representation of an object must occur as it becomes familiar, the nature of this change is not fully understood. In humans, it has been shown that the N170 - an evoked visual potential-is enhanced for classes of objects for which people have visual expertise. In this study, we explored whether monkeys show a similar modulation in event-related potential (ERP) amplitude as a result of long-term familiarity by recording ERPs with chronically implanted electrodes over extended training periods spanning many sessions. In each of 3 experiments, we found larger amplitude visual evoked responses to highly familiar images for the time period of 120-250 ms after stimulus onset. This difference was found when the monkeys were trained in an individual-level discrimination task, in a task that required only color discrimination, and even following a viewing-only task. We thus observed this familiarity effect across several tasks and different object categories and further found that the difference between "familiar" and "novel" became smaller as the animals gained experience with the previously unfamiliar objects across multiple test sessions. These data suggest that changes in visual responses associated with familiarity are evident early in the evoked visual response, are robust, and may be automatic, driven at least in part by repeated object exposure.

DOI： 10.1093/cercor/bhl043

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：PERGAMON-ELSEVIER SCIENCE LTD  

In animals with specialized foveae, eye position has a direct influence over the acquisition of detailed visual information. At the same time, eye movements executed during natural behaviors are closely linked with motor actions. In this study, we investigated patterns of eye movements during a simple visual discrimination task. Three rhesus monkeys learned to recognize images of real world objects with no explicit constraints on eye position. Analysis of the monkeys' eye movements showed that although the endpoint of the initial saccade depended on the particular visual stimulus, the trajectory of the first saccades also reliably predicted the manual response associated with that stimulus. We thus observed that initial saccades executed in a recognition task reflect both perceptual and motor aspects of a visual task. This pattern of eye movements emerged spontaneously in all three animals tested despite the fact that saccades were never explicitly rewarded. As the average saccade latency was under 200 ms, object specific learned associations must have exerted their influence over the initial saccade even earlier, providing a novel temporal marker for the rapidity of visual recognition processes. Taken together, these results suggest that caution should be exercised when interpreting the meaning of oculomotor patterns observed during perceptual tasks, as these blur the line between perceptual processing and motor preparation. (c) 2006 Elsevier Ltd. All rights reserved.

DOI： 10.1016/j.visres.2006.06.009

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：AMER PHYSIOLOGICAL SOC  

Neurons in area TE of the monkey inferior temporal cortex respond selectively to images of particular objects or their characteristic visual features. The mechanism of generation of the stimulus selectivity, however, is largely unknown. This study addresses the role of inhibitory TE neurons in this process by examining their visual response properties and interactions with adjacent target neurons. We applied cross-correlation analysis to spike trains simultaneously recorded from pairs of adjacent neurons in anesthetized macaques. Neurons whose activity preceded a decrease in activity from their partner were presumed to be inhibitory neurons. Excitatory neurons were also identified as the source neuron of excitatory linkage as evidenced by a sharp peak displaced from the 0-ms bin in cross-correlograms. Most inhibitory neurons responded to a variety of visual stimuli in our stimulus set, which consisted of several dozen geometrical figures and photographs of objects, with a clear stimulus preference. On average, 10% of the stimuli increased firing rates of the inhibitory neurons. Both excitatory and inhibitory neurons exhibited a similar degree of stimulus selectivity. Although inhibitory neurons occasionally shared the most preferred stimuli with their target neurons, overall stimulus preferences were less similar between adjacent neurons with inhibitory linkages than adjacent neurons with common inputs and/or excitatory linkages. These results suggest that inhibitory neurons in area TE are activated selectively and exert stimulus-specific inhibition on adjacent neurons, contributing to shaping of stimulus selectivity of TE neurons.

DOI： 10.1152/jn.01267.2003

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Language：English   Publishing type：Research paper (international conference proceedings)   Publisher：SPRINGER-VERLAG TOKYO  

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：MACMILLAN MAGAZINES LTD  

Long-term potentiation (LTP), the increase in synaptic strength evoked by high-frequency stimulation, is often considered to be a cellular model for learning and memory. The validity of this model depends on the assumptions that physiological stimuli can induce LTP in vivo and that the resulting: synaptic modifications correlate with behavioural changes. However, modifiable synapses are generally embedded deep in complex circuits. In contrast, the goldfish Mauthner (M)-cell and its afferent synapses are easily accessible for electrophysiological studies, and firing of this neuron is sufficient to trigger fast escape behaviour in response to sudden stimuli(1,2). We have previously shown that tetanic stimulation can induce LTP of the feedforward inhibitory synapses that control the excitability of the M-ceIl(3,4). Here we report that natural sensory stimulation can induce potentiation of this inhibitory connection that resembles the LTP induced by afferent tetanization. Furthermore, comparable acoustic stimulation produced a parallel decrease in the probability of the sound-evoked escape reflex Thus we demonstrate for the first time, to our knowledge, a behavioural role for the long-term synaptic strengthening of inhibitory synapses.

DOI： 10.1038/28172

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Language：Japanese  

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Language：Japanese   Publisher：日本視覚学会  

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Language：English   Publisher：日本神経化学会  

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Language：English   Publisher：日本神経化学会  

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Language：Japanese   Publisher：The Institute of Electronics, Information and Communication Engineers  

Head movement during video oculography is considered as a major source of artifacts. However, little quantitative information is available as to how pupil detection is affected by head motions. Here we show that the accuracy of pupil detection was significantly higher with head fixation devices than without ones in humans. Moreover, a preliminary study in a macaque monkey indicated that some visual targets on a screen or reward apparatus could improve pupil detection under non head-fixated conditions. These results confirmed the importance of had fixation in video oculography.

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