Yoshiaki Iwamura

Hierarchical somatosensory processing.

Recent studies of the postcentral and additional somatosensory cortices support a hierarchical scheme for information processing. In the postcentral gyrus, the complexity of receptive field properties increases with caudal progression from area 1. It has been reported that the anterior bank of the intraparietal sulcus, the caudalmost part of the postcentral gyrus, is responsible for the systematic integration of bilateral body parts, as well as of somatic and visual information.

Self-images in the video monitor coded by monkey intraparietal neurons.

When playing a video game, or using a teleoperator system, we feel our self-image projected into the video monitor as a part of or an extension of ourselves. Here we show that such a self image is coded by bimodal (somatosensory and visual) neurons in the monkey intraparietal cortex, which have visual receptive fields (RFs) encompassing their somatosensory RFs. We earlier showed these neurons to code the schema of the hand which can be altered in accordance with psychological modification of the body image; that is, when the monkey used a rake as a tool to extend its reach, the visual RFs of these neurons elongated along the axis of the tool, as if the monkeys self image extended to the end of the tool. In the present experiment, we trained monkeys to recognize their image in a video monitor (despite the earlier general belief that monkeys are not capable of doing so), and demonstrated that the visual RF of these bimodal neurons was now projected onto the video screen so as to code the image of the hand as an extension of the self. Further, the coding of the imaged hand could intentionally be altered to match the image artificially modified in the monitor.

Rostrocaudal gradients in the neuronal receptive field complexity in the finger region of the alert monkey's postcentral gyrus.

SummaryIn the primate postcentral gyrus, the cytoarchitectonic characteristics gradually shift from those of koniocortex to more homotypical parakoniocortex along its rostrocaudal axis. To find the physiological correlates of these changes we examined a large body of data accumulated during a series of our experiments with alert monkeys. Along the rostrocaudal axis of the postcentral gyrus, we found a gradual and continuous increase in the number of neurons with converging receptive fields and those in which receptive field positions or submodalities were not determined. Deep or skin submodality neurons were dominant in area 3a or 3b respectively. The proportion of skin submodality neurons decreased gradually from area 3b to the more caudal part of the gyrus. The proportion of deep submodality neurons was almost constant from area 3b to area 2 inclusive; they were not the majority in area 2. The data are consistent with the hierarchical scheme, i.e., within the postcentral gyrus sensory information is processed from the primary sensory receiving stage to the more associative, integrative stages.

Deficits in manipulative behaviors induced by local injections of muscimol in the first somatosensory cortex of the conscious monkey.

Injection of muscimol (GABA agonist) in the finger region of area 2 of the alert monkey led to the striking yet reversible loss of finger coordination, thus disabling the monkey from picking up a small piece of food from a small hole or a funnel. Symptoms varied depending on sites of injection within the finger region. Neither weakness of hand or finger movements nor deficit in hand reach was observed.

Functional subdivisions representing different finger regions in area 3 of the first somatosensory cortex of the conscious monkey

SummaryThe representation of fingers in the first somatosensory cortex was studied in conscious monkeys by recording single neuronal activity, and the following results were obtained:(1)In area 3a, most neurons responded to joint manipulation or other types of deep stimuli. The representation of five fingers was somatotopically arranged.(2)In area 3b, 77.7% and 20.9% of identified neurons responded to cutaneous and deep stimuli respectively.(3)Neurons responding to light mechanical stimuli and with receptive fields on the distal finger segment were found in the most anterior part of area 3b while those responding better to specific mechanical stimuli, such as rubbing, scraping, pinching, tapping, etc. of finger glabrous skin, were found in the more posterior part. The representation of the five fingers was somatotopically arranged.(4)Neurons responding to light or specific mechanical stimulation of the dorsal hairy skin of fingers were found in the posterior part of area 3b. The independent somatotopic representation of four fingers was recognized within this region.(5)Neurons responding to mechanical stimulation of the palmar skin were found in two separate regions, the medial one for the ulnar half and the lateral one for the radial half of the palm.(6)These results indicate that the representation of fingers in areas 3a and 3b of the conscious monkey is divided into multiple somatotopic subdivisions each representing a functional region of the hand and fingers.(7)Neurons with multi-finger receptive fields were occasionally found in area 3b, mostly in layer VI. Some of them had inhibitory receptive fields. Multifinger type receptive fields were more commonly found in area 1.

Converging patterns of finger representation and complex response properties of neurons in area 1 of the first somatosensory cortex of the conscious monkey

SummaryThe representation of the hand and fingers in area 1 of the first somatosensory cortex was studied in conscious monkeys by recording single neuronal activity. The results are as follows.(1)We found multi-finger type receptive fields which cover more than one finger discontinuously or wide-field type ones which cover both finger and palmar skin or two halves of the palmar skin together. Multi-finger type receptive fields were also found in some joint manipulation neurons. Multifinger or wide-field type receptive fields were found in nearly 40% of area 1 neurons. The rate was even higher, up to 70%, in the medial part of the cortical finger region. Consequently, the finger representation in area 1 was less discretely somatotopic than that in area 3b.(2)The submodality content of area 1 was almost identical to that of area 3b: 74.5% and 20.9% of identified neurons were, respectively, cutaneous and deep. The distribution of neurons with different submodalities overlapped in area 1.(3)Among area 1 neurons with multi-finger type receptive fields, response characteristics of those with inhibitory receptive fields, those with directional selectivity to moving stimuli, and those with converging afferent inputs, were studied in detail. Evidence is presented to suggest that information from different parts of the body, or from the same body parts but different afferent sources, is integrated in area 1.(4)It is proposed that, within the SI, area 1 is the initial stage of integration of sensory information coming from the thalamus and from area 3a or 3b via cortico-cortical connections.

Representation of the midline trunk, bilateral arms, and shoulders in the monkey postcentral somatosensory cortex

Abstract Single neuronal activities were recorded in the arm/trunk region of the postcentral gyrus in awake Japanese monkeys. A total of 1608 units were isolated from four hemispheres of two animals, and receptive fields (RFs) and submodalities were identified in 1162 units. Deep or skin submodality neurons were dominant in area 3a or area 3b, respectively. The deep/skin ratio increased as the recording site moved from area 3b to the more caudal areas. In areas 3a and 3b, neuronal RFs were almost exclusively on either the arm or trunk. In areas 2 and 5, neurons with RFs on the trunk decreased and those with RFs on the hand or covering more than one body part, etc. increased. We found a total of 107 neurons with bilateral RFs and 56 with ipsilateral RFs, while the rest (n=999) were with contralateral RFs. Bilateral or ipsilateral neurons of skin submodality (n=37) were found in areas 1, 2, and 5. Twenty six (70%) had RFs on the trunk and/or occiput, five on the forelimb, and the rest (n=6) on both the trunk and forelimb (the combined type). Among 33 skin bilateral neurons, 90% (n=30) had RFs across the midline. Bilateral or ipsilateral neurons responding to joint manipulation (n=104) were found in areas 2 and 5. Most of them were activated by manipulation of the shoulder and/or elbow (the proximal type, n=72, 69%). There were 25 neurons of the combined type (both the proximal and distal joints were effective, 24%). Bilateral or ipsilateral neurons of deep-others submodality (n=20) were found in areas 1, 2, and 5. The forelimb type (n=12, 60%) was dominant in this category. The combined-type neurons in both the skin- and joint-manipulation categories were found only or mostly in area 5. These results indicate the presence of hierarchical processing for bilateral as well as contralateral information within the arm/trunk region of the postcentral gyrus.

Overlapping representation of fingers in the somatosensory cortex (area 2) of the conscious monkey

Finger representation on the first somatosensory cortex was mapped in conscious monkeys by single-unit recording. While representation was somatotopic in area 3, this was not the case in area 2, where the representation of different fingers overlapped. Our results indicate that area 2 is not a pure replica of the receptor sheet of the body surface.

Vertical neuronal arrays in the postcentral gyrus signaling active touch: a receptive field study in the conscious monkey

SummarySingle neuronal activity was recorded in the crown of the postcentral gyrus (areas 1 and 2) in 5 conscious monkeys. A total of 88 penetrations entered perpendicularly to the cortical surface. Among them, 6 examples are chosen and the receptive field characteristics of constituent neurons were described in some detail. Receptive fields of neurons recorded along a particular penetration were variable in their positions, but the largest receptive field usually covered the others. Neurons with the largest receptive fields were found most frequently in the infragranular layers. Often they included inhibitory receptive fields. The inhibitory receptive fields were arranged side-by-side to the excitatory ones, rather than in a center-surround fashion. The key stimulus common to neurons in a vertical penetration was the contact of an object to the receptive field achieved during animals active behavior to manipulate the object. We thus designated the largest receptive field as a functional surface. Our results demonstrate that a vertical array of neurons in this cortical region can be regarded as a functional assemblage which deals with a set of information concerning one of various aspects of active touch.

Processing of tactile and kinesthetic signals from bilateral sides of the body in the postcentral gyrus of awake monkeys

Earlier studies pointed out that in the primary somatosensory cortex (SI) the receptive fields (RF) of bilateral neurons were related exclusively to the body midline. We recently found a substantial number of neurons with bilateral RFs on hand digits, shoulders/arms or legs/feet in the caudalmost part (areas 2 and 5) of the postcentral gyrus in awake macaque monkeys. The RFs of these neurons were generally of the most complex types found in this region of the cortex, and thus they were considered to be at the highest level along the hierarchical chain of information processing. We conclude that there are two types of bilateral RFs in the postcentral gyrus, one representing the midline structures such as the intraoral cavity, chin or trunk and the other related to limb structures such as fingers, hands, arms, shoulders, legs and girdles. Functional significance of the bilateral activity could be understood in behavioral context as it is seen more extensively in the body parts where bilateral coordination is essential.