Sayaka Hihara

Extension of corticocortical afferents into the anterior bank of the intraparietal sulcus by tool-use training in adult monkeys

When humans use a tool, it becomes an extension of the hand physically and perceptually. Common introspection might occur in monkeys trained in tool-use, which should depend on brain operations that constantly update and automatically integrate information about the current intrinsic (somatosensory) and the extrinsic (visual) status of the body parts and the tools. The parietal cortex plays an important role in using tools. Intraparietal neurones of naïve monkeys mostly respond unimodally to somatosensory stimuli; however, after training these neurones become bimodally active and respond to visual stimuli. The response properties of these neurones change to code the body images modified by assimilation of the tool to the hand holding it. In this study, we compared the projection patterns between visually related areas and the intraparietal cortex in trained and naïve monkeys using tracer techniques. Light microscopy analyses revealed the emergence of novel projections from the higher visual centres in the vicinity of the temporo-parietal junction and the ventrolateral prefrontal areas to the intraparietal area in monkeys trained in tool-use, but not in naïve monkeys. Functionally active synapses of intracortical afferents arising from higher visual centres to the intraparietal cortex of the trained monkeys were confirmed by electron microscopy. These results provide the first concrete evidence for the induction of novel neural connections in the adult monkey cerebral cortex, which accompanies a process of demanding behaviour in these animals.

Acquisition and development of monkey tool-use: behavioral and kinematic analyses.

Four Japanese macaques were trained in the use of a T-shaped rake. Use the tool and development of the level of the skill of tool-use took place in three distinct stages. During stage 1, two of the monkeys seemed to use insight for initial solution, while fortuitous experiences led the other two monkeys to the solution. All the monkeys used the tool in a stereotyped manner and could retrieve food only when the tool was placed close to the food. At stage 2 the monkeys became able to manipulate the tool in various ways and became able to retrieve the food regardless of its position. By stage 3 they had developed the level of skill required for efficient retrieval. Further experiments revealed that the monkeys attempted to use unfamiliar objects which were similar to the original tool in shape, but not spherical or ring-shaped objects, to rake in the food.

Tool-use learning induces BDNF expression in a selective portion of monkey anterior parietal cortex

Learning but not execution of tool-use induced expression of brain-derived neurotrophic factor (BDNF). The expression was highest in the anterior bank of the intraparietal sulcus, especially in the region posteriorly adjacent to the somatosensory shoulder and forearm region in area 3b, suggesting that BDNF plays a role in altering the body image of the hand to include the repeatedly used tool as its extension.

Tool-use learning selectively induces expression of brain-derived neurotrophic factor, its receptor trkB, and neurotrophin 3 in the intraparietal multisensorycortex of monkeys.

When humans repeatedly use a tool, our body image alters until the tool finally becomes a part or an extension of the body. This alteration of body image perhaps results from re-integration of somatosensory and visual signals. We trained Japanese monkeys to use a rake-shaped tool to retrieve a distant food pellet, then used a novel tissue-sampling method to suction brain tissue from the anterior bank of their intraparietal sulcus, where somatosensory and visual signals converge. Examination of the messenger RNA expression levels of neurotrophins and their receptors using real-time quantitative polymerase chain reaction revealed learning-selective induction in the expression of brain-derived neurotrophic factor, its receptor trkB, and NT-3 during, but not after, the learning. These results suggest that these factors are involved in the reorganization of the somatosensory and visual signals in the anterior bank of the intraparietal sulcus when monkeys are learning the use of the tool.

Dynamic social adaptation of motion-related neurons in primate parietal cortex

Social brain function, which allows us to adapt our behavior to social context, is poorly understood at the single-cell level due largely to technical limitations. But the questions involved are vital: How do neurons recognize and modulate their activity in response to social context? To probe the mechanisms involved, we developed a novel recording technique, called multi-dimensional recording, and applied it simultaneously in the left parietal cortices of two monkeys while they shared a common social space. When the monkeys sat near each other but did not interact, each monkeys parietal activity showed robust response preference to action by his own right arm and almost no response to action by the others arm. But the preference was broken if social conflict emerged between the monkeys—specifically, if both were able to reach for the same food item placed on the table between them. Under these circumstances, parietal neurons started to show complex combinatorial responses to motion of self and other. Parietal cortex adapted its response properties in the social context by discarding and recruiting different neural populations. Our results suggest that parietal neurons can recognize social events in the environment linked with current social context and form part of a larger social brain network.

Tool-use training in a species of rodent: the emergence of an optimal motor strategy and functional understanding.

Background Tool use is defined as the manipulation of an inanimate object to change the position or form of a separate object. The expansion of cognitive niches and tool-use capabilities probably stimulated each other in hominid evolution. To understand the causes of cognitive expansion in humans, we need to know the behavioral and neural basis of tool use. Although a wide range of animals exhibit tool use in nature, most studies have focused on primates and birds on behavioral or psychological levels and did not directly address questions of which neural modifications contributed to the emergence of tool use. To investigate such questions, an animal model suitable for cellular and molecular manipulations is needed. Methodology/Principal Findings We demonstrated for the first time that rodents can be trained to use tools. Through a step-by-step training procedure, we trained degus (Octodon degus) to use a rake-like tool with their forelimbs to retrieve otherwise out-of-reach rewards. Eventually, they mastered effective use of the tool, moving it in an elegant trajectory. After the degus were well trained, probe tests that examined whether they showed functional understanding of the tool were performed. Degus did not hesitate to use tools of different size, colors, and shapes, but were reluctant to use the tool with a raised nonfunctional blade. Thus, degus understood the functional and physical properties of the tool after extensive training. Conclusions/Significance Our findings suggest that tool use is not a specific faculty resulting from higher intelligence, but is a specific combination of more general cognitive faculties. Studying the brains and behaviors of trained rodents can provide insights into how higher cognitive functions might be broken down into more general faculties, and also what cellular and molecular mechanisms are involved in the emergence of such cognitive functions.

Social cognition in premotor and parietal cortex

Abstract Socially correct behavior requires constant observation of the social environment. Behavior that was appropriate a few seconds ago is not guaranteed to be appropriate now. The brain keeps the eyes focused on the current social space and constantly updates its internal representation of the environment and social context. Monitoring the behavior of others is essential for this updating. The neural systems involved in perceiving the actions of others have been explored extensively, but the detailed, quantitative character of the system at the single-cell level remains poorly understood. To address this question, we used the new technique of multidimensional recording to record neuronal activity in monkeys simultaneously from ventral premotor cortex (PM) and parietal cortex in the left hemisphere while they performed a food grab task. Motion-related (MR) response was shown by 35% (52/148) of PM neurons and 54% (94/174) of parietal neurons, meaning their activity increased in response to various combinations of arm motions made by self and/or other. Both areas showed robust lateralized preference to Self–Right action. When it came to recognizing the actions of the other monkey, PM-MR neurons showed the same kind of right-arm preference as self-action while parietal-MR neurons, in contrast, did not show arm preference. And while both areas discriminated self-action from other, a significantly larger proportion of PM-MR neurons did so. These results suggest that PM neurons provide information about an actions agent and effector as primitives of action cognition within the mirror neuron network, while parietal neurons represent social space and participate in the recognition of another agents actions in relation to ones own actions within the parieto-prefrontal network.

Spontaneous vocal differentiation of coo-calls for tools and food in Japanese monkeys.

Vocal production and its usage in nonhuman primates may share common features with primitive human language. We trained two Japanese monkeys to use a rake-shaped tool to retrieve distant food. After the training, the monkeys spontaneously began vocalizing coo-calls in the tool-using context. We then trained one of the monkeys to vocalize to request food or the tool. Three independent acoustic parameters were measured and each parameter was independently analyzed across conditions using a multiple comparison test. We found that the monkey spontaneously differentiated their coo-calls to ask for either food or tool during the course of this training. This process might involve a change from emotional vocalizations into intentionally controlled ones by associating them with consciously planned tool use. We thus established a novel hypothesis about the origin of voluntary vocal control that could be approached from neurophysiological procedures.

Social state representation in prefrontal cortex

Abstract One of the cardinal mental faculties of humans and other primates is social brain function, the collective name assigned to the distributed system of social cognitive processes that orchestrate our sophisticated adaptive social behavior. These must include processes for recognizing current social context and maintaining an internal representation of the current social state as a reference for decision-making. But how and where the brain processes such social-state information is unknown. To home in on the neural substrates of social-state representation, the activity of 196 prefrontal (PFC) neurons was recorded from two monkeys simultaneously during a food-grab task under varying social conditions. Of PFC neurons, 39% showed activity modulation during movement-free periods and seemed to be representing current social state. The direction of modulation was opposite between the dominant and submissive monkeys: During social engagement, PFC activity increased in the dominant monkey and was suppressed in the submissive monkey. The modulation was consistently observed in additional PFC neurons (27/72) in additional pairings with two other monkeys. Notably, PFC activity in one formerly submissive monkey switched to dominant modulation mode when he was paired with a new monkey of lower social status. These findings suggest that PFC, as part of a larger social brain network, maintains a multistate classification of social context for use as a behavioral reference for social decision-making.

Visual Responsiveness of Neurons in the Secondary Somatosensory Area and its Surrounding Parietal Operculum Regions in Awake Macaque Monkeys

Previous neurophysiological studies performed in macaque monkeys have shown that the secondary somatosensory cortex (SII) is essentially engaged in the processing of somatosensory information and no other sensory input has been reported. In contrast, recent human brain-imaging studies have revealed the effects of visual and auditory stimuli on SII activity, which suggest multisensory integration in the human SII. To determine whether multisensory responses of the SII also exist in nonhuman primates, we recorded single-unit activity in response to visual and auditory stimuli from the SII and surrounding regions in 8 hemispheres from 6 awake monkeys. Among 1157 recorded neurons, 306 neurons responded to visual stimuli. These visual neurons usually responded to rather complex stimuli, such as stimulation of the peripersonal space (40.5%), observation of human action (29.1%), and moving-object stimulation outside the monkeys reach (23.9%). We occasionally applied auditory stimuli to visual neurons and found 10 auditory-responsive neurons that exhibited somatosensory responses. The visual neurons were distributed continuously along the lateral sulcus covering the entire SII, along with other somatosensory neurons. These results highlight the need to investigate novel functional roles—other than somesthetic sensory processing—of the SII.