Miki Taoka

Triadic (ecological, neural, cognitive) niche construction: a scenario of human brain evolution extrapolating tool use and language from the control of reaching actions

Hominin evolution has involved a continuous process of addition of new kinds of cognitive capacity, including those relating to manufacture and use of tools and to the establishment of linguistic faculties. The dramatic expansion of the brain that accompanied additions of new functional areas would have supported such continuous evolution. Extended brain functions would have driven rapid and drastic changes in the hominin ecological niche, which in turn demanded further brain resources to adapt to it. In this way, humans have constructed a novel niche in each of the ecological, cognitive and neural domains, whose interactions accelerated their individual evolution through a process of triadic niche construction. Human higher cognitive activity can therefore be viewed holistically as one component in a terrestrial ecosystem. The brains functional characteristics seem to play a key role in this triadic interaction. We advance a speculative argument about the origins of its neurobiological mechanisms, as an extension (with wider scope) of the evolutionary principles of adaptive function in the animal nervous system. The brain mechanisms that subserve tool use may bridge the gap between gesture and language—the site of such integration seems to be the parietal and extending opercular cortices.

Book Review: Bilateral Activity and Callosal Connections in the Somatosensory Cortex

Earlier studies recording single neuronal activity in the postcentral somatosensory cortex of monkeys converged in suggesting that the bilateral receptive fields were related exclusively to the body midline including the trunk, perioral face, and oral cavity. These neurons were recorded mostly in the rostral part of the gyrus, areas 3b and 1. However, the authors recently found a substantial number of neurons with bilateral receptive fields on extremities, hand/digits, shoulders/arms, or legs/feet in the caudalmost part (areas 2 and 5) of the postcentral gyrus. The authors review these results and discuss functional implications of the bilateral representation in the postcentral somatosensory cortex.

Hand before foot? Cortical somatotopy suggests manual dexterity is primitive and evolved independently of bipedalism

People have long speculated whether the evolution of bipedalism in early hominins triggered tool use (by freeing their hands) or whether the necessity of making and using tools encouraged the shift to upright gait. Either way, it is commonly thought that one led to the other. In this study, we sought to shed new light on the origins of manual dexterity and bipedalism by mapping the neural representations in the brain of the fingers and toes of living people and monkeys. Contrary to the ‘hand-in-glove’ notion outlined above, our results suggest that adaptations underlying tool use evolved independently of those required for human bipedality. In both humans and monkeys, we found that each finger was represented separately in the primary sensorimotor cortex just as they are physically separated in the hand. This reflects the ability to use each digit independently, as required for the complex manipulation involved in tool use. The neural mapping of the subjects’ toes differed, however. In the monkeys, the somatotopic representation of the toes was fused, showing that the digits function predominantly as a unit in general grasping. Humans, by contrast, had an independent neurological representation of the big toe (hallux), suggesting association with bipedal locomotion. These observations suggest that the brain circuits for the hand had advanced beyond simple grasping, whereas our primate ancestors were still general arboreal quadrupeds. This early adaptation laid the foundation for the evolution of manual dexterity, which was preserved and enhanced in hominins. In hominins, a separate adaptation, involving the neural separation of the big toe, apparently occurred with bipedality. This accords with the known fossil evidence, including the recently reported hominin fossils which have been dated to 4.4 million years ago.

Periostin, a neurite outgrowth-promoting factor, is expressed at high levels in the primate cerebral cortex

Periostin (POSTN or osteoblast specific factor) is an extracellular matrix protein originally identified as a protein highly expressed in osteoblasts. Recently, periostin has been reported to function in axon regeneration and neuroprotection. In the present study, we focused on periostin function in cortical evolution. We performed a comparative gene expression analysis of periostin between rodents (mice) and primates (marmosets and macaques). Periostin was expressed at higher levels in the primate cerebral cortex compared to the mouse cerebral cortex. Furthermore, we performed overexpression experiments of periostin in vivo and in vitro. Periostin exhibited neurite outgrowth activity in cortical neurons. These results suggested the possibility that prolonged and increased periostin expression in the primate cerebral cortex enhances the cortical plasticity of the mammalian cerebral cortex.

Identification of tool use acquisition‐associated genes in the primate neocortex

Japanese macaques are able to learn how to use rakes to take food after only a few weeks of training. Since tool‐use training induced rapid morphological changes in some restricted brain areas, this system will be a good model for studying the neural basis of plasticity in human brains. To examine the mechanisms of tool‐use associated brain expansion on the molecular and cellular level, here, we performed comprehensive analysis of gene expressions with microarray. We identified various transcripts showing differential expression between trained and untrained monkeys in the region around the lateral and intraparietal sulci. Among candidates, we focused on genes related to synapse formation and function. Using quantitative reverse transcription–polymerase chain reaction and histochemical analysis, we confirmed at least three genes (ADAM19, SPON2, and WIF1) with statistically different expression levels in neurons and glial cells. Comparative analysis revealed that tool use‐associated genes were more obviously expressed in macaque monkeys than marmosets or mice. Thus, our findings suggest that cognitive tasks induce structural changes in the neocortex via gene expression, and that learning‐associated genes innately differ with relation to learning ability.

Modulation of cortical vestibular processing by somatosensory inputs in the posterior insula

Abstract Primary objective: To study the mechanism of somatosensory-vestibular interactions, this study examined the effects of somatosensory inputs on body sway induced by galvanic vestibular stimulation (GVS) in healthy participants and persons with brain injury in the posterior insula, a region constituting a part of the parietoinsular vestibular cortex. Research design: This study adopted an experimental, controlled, repeated measures design. Methods and procedures: Participants were 11 healthy individuals, two persons with unilateral posterior insular injury and two age-matched controls. Bipolar GVS was applied to the mastoid processes while participants were sitting with their eyes closed, either lightly touching a stable surface with their index finger or not touching the surface with their index finger. Main outcomes and results: In healthy participants, tilting was greater with right hemispheric stimulation than with left hemispheric stimulation. Moreover, with right hemispheric stimulation, tilting was greater with a right finger touch than with no touch. The person with right-brain injury showed tilting induced by GVS; however, finger touch had no modulatory effect. In contrast, finger touch enhanced tilting in the person with left-brain injury. Conclusions: These preliminary results are discussed in light of a hypothesis of right hemispheric dominance of somatosensory-vestibular interactions in the posterior insula.

Rapid identification of cortical motor areas in rodents by high-frequency automatic cortical stimulation and novel motor threshold algorithm

Cortical stimulation mapping is a valuable tool to test the functional organization of the motor cortex in both basic neurophysiology (e.g., elucidating the process of motor plasticity) and clinical practice (e.g., before resecting brain tumors involving the motor cortex). However, compilation of motor maps based on the motor threshold (MT) requires a large number of cortical stimulations and is therefore time consuming. Shortening the time for mapping may reduce stress on the subjects and unveil short-term plasticity mechanisms. In this study, we aimed to establish a cortical stimulation mapping procedure in which the time needed to identify a motor area is reduced to the order of minutes without compromising reliability. We developed an automatic motor mapping system that applies epidural cortical surface stimulations (CSSs) through one-by-one of 32 micro-electrocorticographic electrodes while examining the muscles represented in a cortical region. The next stimulus intensity was selected according to previously evoked electromyographic responses in a closed-loop fashion. CSS was repeated at 4 Hz and electromyographic responses were submitted to a newly proposed algorithm estimating the MT with smaller number of stimuli with respect to traditional approaches. The results showed that in all tested rats (n = 12) the motor area maps identified by our novel mapping procedure (novel MT algorithm and 4-Hz CSS) significantly correlated with the maps achieved by the conventional MT algorithm with 1-Hz CSS. The reliability of the both mapping methods was very high (intraclass correlation coefficients ≧0.8), while the time needed for the mapping was one-twelfth shorter with the novel method. Furthermore, the motor maps assessed by intracortical microstimulation and the novel CSS mapping procedure in two rats were compared and were also significantly correlated. Our novel mapping procedure that determined a cortical motor area within a few minutes could help to study the functional significance of short-term plasticity in motor learning and recovery from brain injuries. Besides this advantage, particularly in the case of human patients or experimental animals that are less trained to remain at rest, shorter mapping time is physically and mentally less demanding and might allow the evaluation of motor maps in awake individuals as well.

Neurons that become active during hand and mouth movements in the hand region of the secondary somatosensory cortex of the macaque monkey

The expression of c-fos gene in catecholaminergic neurons within the brainstem was examined immunohistochemically. Conscious animals were subjected to eccentric rotation on the horizontal plane. Neuronal activation was defined by Fos protein expression. After stimulation, the Fos protein were mainly distributed in the vestibular nucleus complex (VNC), parabrachial nucleus (PBN), nucleus of the solitary tract (NTS), locus coeruleus (LC), substantia nigra (SN), caudoor rostro-ventrolateral reticular formation (CVL, RVL), etc. Double immunofluorescent staining showed that most of catecholaminergic neurons in the NTS were activation (double labeled Fos/TH neurons) after eccentric rotation. Double labeled Fos/TH neurons were also observed in LC, CVL, RVL, and other regions related to sympathetic activities of the brainstem. However, there were no double labeled Fos/TH neurons in the SN. Our findings suggest that the catecholaminergic neurons in the brainstem may contribute to the changes of the sympathetic activities induced by the gravity-related spatial information during head movements.

Neuronal receptive fields covering multiple body parts in the second somatosensory cortex of awake macaque monkeys

We previously reported the presence of neurons with large receptive fields (RFs) covering multiple body parts such as the head (including the face or mouth), forelimb, hindlimb and/or trunk in the second somatosensory cortex (SII). Of 256 neurons with such RFs from SII of awake macaque monkeys, we investigated their response properties and distribution pattern. Most of them were driven bilaterally (N=229, 89%). These neurons were classified into two groups according to their RFs whether they included the tnmk (the trunk type, N=124) or not (the extremity type, N=l32). The majority of the tnmk type had RFs extending into the forelimb, hindlimb and/or head continuously (N= 117, 94%). RFs of 54 neurons of them covered almost the whole body. Most of the extremity type had RFs combining the hand, foot and/or mouth (N=82, 62%). On the unfolded map of SII, these two types were differentially distributed; most of the trunk type were in the lateral half of SII and most of the extremity type in the medial half of SII suggesting that the two parts of SII could functionally be differentiated.

1808 Bilateral/ipsilateral neurons in the arm/trunk region of the monkey postcentral somatosensory cortex

JUN SATO, TAKAO KUMAZAWA, KAZUE MIZUMURA We have previously reported that norepinephrine (NE) sensitizes bradykinin (BK) response of cutaneous polymodal receptors (CPR) putatively involving cutaneous pain. Now the effect of NE on the heat response of CPR was studied using a rat skin-saphenous nerve in vitro preparation. Receptive fields of identified single CPR units were isolated and superfused at the corium side with NE solution. Ramp heat stimulation was repeatedly applied to the isolated receptive field at lo-min intervals with a radiant heat stimulator. NE (l-1OpM) by itself did not excite CPRs before the first heat exposure. In contrast, after a few heating trials, some CPR units were excited by NE. The heat response was clearly suppressed by NE regardless of the presence of NE-induced excitation. Present results combined with previous results on the BK response suggest a different mechanism of NEmodification on BK and heat responses.