Bilateral Receptive Fields Research Articles

Functional Relevance of Dual Olfactory Bulbs in Olfactory Coding.

Bilateral convergence of external stimuli is a common feature of vertebrate sensory systems. This convergence of inputs from the bilateral receptive fields allows higher order sensory perception, such as depth perception in the vertebrate visual system and stimulus localization in the auditory system. The functional role of such bilateral convergence in the olfactory system is unknown. To test whether each olfactory bulb (OB) contributes a separate piece of olfactory information, and whether information from the bilateral OB is integrated, we synchronized the activation of OBs with blue light in mice expressing ChIEF in the olfactory sensory neurons (OSNs) and behaviorally assessed the relevance of dual OBs in olfactory perception. Our findings suggest that each OB contributes separate components of olfactory information, and the mice integrate the bilaterally synchronized olfactory information for olfactory identity.

Neural encoding of actual and imagined touch within human posterior parietal cortex.

In the human posterior parietal cortex (PPC), single units encode high-dimensional information with partially mixed representations that enable small populations of neurons to encode many variables relevant to movement planning, execution, cognition, and perception. Here, we test whether a PPC neuronal population previously demonstrated to encode visual and motor information is similarly engaged in the somatosensory domain. We recorded neurons within the PPC of a human clinical trial participant during actual touch presentation and during a tactile imagery task. Neurons encoded actual touch at short latency with bilateral receptive fields, organized by body part, and covered all tested regions. The tactile imagery task evoked body part-specific responses that shared a neural substrate with actual touch. Our results are the first neuron-level evidence of touch encoding in human PPC and its cognitive engagement during a tactile imagery task, which may reflect semantic processing, attention, sensory anticipation, or imagined touch.

Binocular Encoding in the Damselfly Pre-motor Target Tracking System.

Akin to all damselflies, Calopteryx (family Calopterygidae), commonly known as jewel wings or demoiselles, possess dichoptic (separated) eyes with overlapping visual fields of view. In contrast, many dragonfly species possess holoptic (dorsally fused) eyes with limited binocular overlap. We have here compared the neuronal correlates of target tracking between damselfly and dragonfly sister lineages and linked these changes in visual overlap to pre-motor neural adaptations. Although dragonflies attack prey dorsally, we show that demoiselles attack prey frontally. We identify demoiselle target-selective descending neurons (TSDNs) with matching frontal visual receptive fields, anatomically and functionally homologous to the dorsally positioned dragonfly TSDNs. By manipulating visual input using eyepatches and prisms, we show that moving target information at the pre-motor level depends on binocular summation in demoiselles. Consequently, demoiselles encode directional information in a binocularly fused frame of reference such that information of a target moving toward the midline in the left eye is fused with information of the target moving away from the midline in the right eye. This contrasts with dragonfly TSDNs, where receptive fields possess a sharp midline boundary, confining responses to a single visual hemifield in a sagittal frame of reference (i.e., relative to the midline). Our results indicate that, although TSDNs are conserved across Odonata, their neural inputs, and thus the upstream organization of the target tracking system, differ significantly and match divergence in eye design and predatory strategies. VIDEO ABSTRACT.

A systematic analysis of neurons with large somatosensory receptive fields covering multiple body regions in the secondary somatosensory area of macaque monkeys.

Previous neurophysiological studies performed in macaque monkeys have revealed complex somatosensory responses in the secondary somatosensory area (SII), such as large receptive fields (RFs), as well as bilateral ones. However, systematic analyses of neurons with large RFs have not been performed. In the present study, we recorded single-unit activities in SII of awake macaque monkeys to investigate systematically large RFs by dividing the whole body into four body regions (head, trunk, forelimb, and hindlimb). Recorded neurons were classified into two types, according to whether the RFs were confined to one body region: single (n = 817) and combined (n = 282) body-region types. These two types were distinct in terms of the percentage of bilateral RFs: 55% in the single-region type and 90% in the combined type, demonstrating that two types of RF enlargement occur simultaneously in the combined type, namely, RF convergence from different body regions and RF convergence from both hemibodies. Among the combined-type RFs, two tendencies of RF convergence were found: 1) the distal parts of the limbs (i.e., hand and foot) and the mouth are interconnected, and 2) the trunk RFs extend continuously toward the distal parts of the limb and head to cover the entire body surface. Our distribution analysis on unfolded maps clarified that neurons having RFs with these two tendencies were distributed within specific subregions in SII.

Receptive field characteristics of stretch-insensitive mechanosensitive units in the rat urinary bladder

The pelvic, hypogastric and pudendal nerves carry sensory information from the urinary bladder. The pelvic nerve is reported to be the most important one of these afferent nerves in producing urinary bladder sensation. The primary types of mechanoreceptors in the bladder can be divided into stretch-sensitive and stretch-insensitive units. The former is considered to be more important in producing bladder sensation. However, little is known about the precise receptive field properties of the stretch-insensitive mechanoreceptors in the urinary bladder. Therefore, in this study, we systematically investigated the receptive field characteristics of the pelvic single unit innervating the rat bladder wall. Functional single unit recordings were made from the pelvic nerve afferent filaments of anesthetized rats. A von Frey device was used for quantitative mechanical stimulation of the bladder surface. In addition, electrical stimulation was used for estimating conduction velocities of the nerve fibers in the receptive field. The threshold value for mechanical stimulation was statistically lower at the caudal portion of the bladder body (sites IV and V) than the other bladder sites. The bladder neck (site I) had the highest mechanical stimulation threshold value for the bladder stretch-insensitive mechanoreceptors. In most cases, the pelvic nerve had bilateral receptive fields. The majority of the pelvic nerve afferents had conduction velocities in the slow A-δ or C fiber range. Mechanical stimulation threshold values were higher in males than in females in a portion of the bladder sites. The pelvic stretch-insensitive bladder mechanoreceptors are 1) higher threshold at the bladder base, 2) contain large bilateral receptive fields and 3) demonstrate relatively slow conduction velocities. These characteristics indicate a non-uniform distribution of stretch-insensitive mechanoreceptors in the rat urinary bladder wall.

Plasticity and Stability of the Visual System in Human Achiasma

The absence of the optic chiasm is an extraordinary and extreme abnormality in the nervous system. The abnormality produces highly atypical functional responses in the cortex, including overlapping hemifield representations and bilateral population receptive fields in both striate and extrastriate visual cortex. Even in the presence of these large functional abnormalities, the effect on visual perception and daily life is not easily detected. Here, we demonstrate that in two achiasmic humans the gross topography of the geniculostriate and occipital callosal connections remains largely unaltered. We conclude that visual function is preserved by reorganization of intracortical connections instead of large-scale reorganizations of the visual cortex. Thus, developmental mechanisms of local wiring within cortical maps compensate for the improper gross wiring to preserve function in human achiasma.

Representation of the Ipsilateral Visual Field by Neurons in the Macaque Lateral Intraparietal Cortex Depends on the Forebrain Commissures

Our eyes are constantly moving, allowing us to attend to different visual objects in the environment. With each eye movement, a given object activates an entirely new set of visual neurons, yet we perceive a stable scene. One neural mechanism that may contribute to visual stability is remapping. Neurons in several brain regions respond to visual stimuli presented outside the receptive field when an eye movement brings the stimulated location into the receptive field. The stored representation of a visual stimulus is remapped, or updated, in conjunction with the saccade. Remapping depends on neurons being able to receive visual information from outside the classic receptive field. In previous studies, we asked whether remapping across hemifields depends on the forebrain commissures. We found that, when the forebrain commissures are transected, behavior dependent on accurate spatial updating is initially impaired but recovers over time. Moreover, neurons in lateral intraparietal cortex (LIP) continue to remap information across hemifields in the absence of the forebrain commissures. One possible explanation for the preserved across-hemifield remapping in split-brain animals is that neurons in a single hemisphere could represent visual information from both visual fields. In the present study, we measured receptive fields of LIP neurons in split-brain monkeys and compared them with receptive fields in intact monkeys. We found a small number of neurons with bilateral receptive fields in the intact monkeys. In contrast, we found no such neurons in the split-brain animals. We conclude that bilateral representations in area LIP following forebrain commissures transection cannot account for remapping across hemifields.

Somatotopic organization of pain responses to direct electrical stimulation of the human insular cortex

The question whether pain encoding in the human insula shows some somatotopic organization is still pending. We studied 142 patients undergoing depth stereotactic EEG (SEEG) exploration of the insular cortex for pre-surgical evaluation of epilepsy. 472 insular electrical stimulations were delivered, of which only 49 (10.5%) elicited a painful sensation in 38 patients (27%). Most sites where low intensity electric stimulation produced pain, without after-discharge or concomitant visually detectable change in EEG activity outside the insula, were located in the posterior two thirds of the insula. Pain was located in a body area restricted to face, upper limb or lower limb for 27 stimulations (55%) and affected more than one of these regions for all others. The insular cortex being oriented parallel to the medial sagittal plane we found no significant difference between body segment representations in the medio-lateral axis. Conversely a somatotopic organization of sites where stimulation produced pain was observed along the rostro-caudal and vertical axis of the insula, showing a face representation rostral to those of upper and lower limbs, with an upper limb representation located above that of the lower limb. These data suggest that, in spite of large and often bilateral receptive fields, pain representation shows some degree of somatotopic organization in the human insula.

Bilateral long-range interaction between right and left visual hemifield

Long-range interaction has been reported to be limited in space within a few degrees. Here, we present a new type of interaction by means of a bilateral configuration using two Gabor signals (GSs). Two horizontally oriented GSs, the first defined as a cue and the second as a probe, appeared in the right and left peripheral visual fields in mirror symmetrical regions. The detection threshold of the GS probe was found to decrease significantly up to cue-probe separations of 10 degrees tested. Since the interaction was sensitive to symmetrical locus, as well as specific to the direction of the horizontal axis, the results suggest novel long-range interaction extending toward the periphery with a mirror-symmetrical configuration. This may be acquired by neuronal communication, which directly connects bilateral receptive fields in the right and left visual cortices.

Sensory Neuroscience: From Skin to Object in the Somatosensory Cortex

Humans can perceive the shape of objects by touch alone, by extracting geometric features such as edges. Recently recorded responses of single neurons in the secondary somatosensory cortex of monkeys suggest how the brain integrates tactile shape information across different regions of skin and builds up a representation of tactile objects.

Reliable detection of bilateral activation in human primary somatosensory cortex by unilateral median nerve stimulation

In non-human primates, a bilateral representation of unilaterally presented somatosensory information can be found at the lowest level of cortical processing as indicated by the presence of neurons with bilateral receptive fields in the hand region of primary somatosensory (SI) cortex. In humans, such bilateral activation of SI is considered controversial due to highly variable detection rates for the much weaker ipsilateral response across different studies (ranging from 3% to 100%). Second-order blind identification (SOBI) is a blind source separation algorithm that has been successfully used to isolate neuronal signals from functionally distinct brain regions, including the left- and right-SI. SOBI-aided extraction of left- and right-SI responses to median nerve stimulation from high-density EEG has been previously validated against the fMRI and MEG literature. Here, we applied SOBI to EEG data and examined whether relatively weaker ipsilateral activations could be reliably detected across subjects. In single subject analysis, statistically significant somatosensory evoked potentials (SEPs) in response to unilateral stimulation were detected from both SI contralateral to and SI ipsilateral to the side of stimulation. Furthermore, these ipsilateral responses were observed in both the left and right hemispheres of all 10 subjects studied. Together these results demonstrate that unilateral stimulation of the median nerve, whether applied to the left or right wrist, can activate both the left- and right-SI, raising the possibility that in humans, unilateral sensory input may be bilaterally represented at the lowest level of cortical processing.

Localization of the human female breast in primary somatosensory cortex

Despite an extensive body of research on the topography of the primary somatosensory cortex (S1) little is known about the representation of the trunk. The aim of this study was to determine the representation of the breast in S1 in human females. The representation of the human breast in primary somatosensory cortex was determined in ten healthy female subjects. Non-painful electrical stimulation of the mammilla (Th4 dermatome), groin (L1 dermatome) and the first digit of both sides of the body activated cutaneous receptors and thus elicited somatosensory evoked potentials. The representation of these body parts in primary somatosensory cortex (S1) was determined using neuroelectric source imaging. Equivalent current dipole localizations were overlaid with individual structural magnetic resonance images to account for individual cortical differences. The breast representation was localized between the representation of the groin and the first digit. In the medial-lateral direction the representation of the breast was approximately 15 mm lateral of the longitudinal fissure in the contralateral hemisphere. Source localizations were stable across subjects. However, one subject showed ipsilateral representation of the breast, which might be related to bilateral receptive fields of the ventral body midline representation. This study confirms the Penfield and Rasmussen (1950) invasive data by use of noninvasive source imaging.

Visceral nociceptive input to the area of the medullary lateral reticular nucleus ascends in the lateral spinal cord

In halothane-anesthetized rats, neurons stereotaxically located in the region of the medullary lateral reticular nucleus (LRN) and responsive to urinary bladder distension (UBD) were characterized using extracellular electrodes. Most neurons excited by UBD were also excited by noxious stimuli applied to bilateral receptive fields comprising at least half of the body surface. These bilateral nociceptive specific (bNS) neurons exhibited graded responses to graded intensities of UBD. Neuronal responses to noxious UBD were highly positively correlated with responses to noxious colorectal distension, suggesting a convergence of visceral sensory information in the area of LRN. Bilateral lateral mid-cervical spinal cord lesions virtually abolished activity of bNS neurons evoked by noxious UBD, while dorsal midline lesions had no significant effect. These data support a role for neurons in the region of the LRN in visceral nociception and implicate traditional lateral spinal cord pain pathways in the transmission of visceral information to caudal ventrolateral medullary structures.

Converging patterns of inputs from oral structures in the postcentral somatosensory cortex of conscious macaque monkeys.

Single neuronal activities were recorded in the oral region of the postcentral gyrus in conscious Japanese monkeys. Among 5,756 neurons isolated, receptive fields (RFs) and submodalities were identified in 1,502 neurons in area 3b, 970 in area 1, and 1,461 in area 2. The relative incidence of neurons that had bilateral RFs increased gradually upon moving caudally from area 3b to area 2 (bilateral integration). A total of 276 neurons had bimaxillary RFs covering both the maxillary and mandibular divisions of the trigeminal nerve, such as the upper and lower lips, upper and lower teeth, palate and tongue, or combinations thereof. There was also a tendency for the relative incidence of neurons with bimaxillary RFs to increase across the postcentral gyrus but with an abrupt change in area 2 (bimaxillary integration). A total of 382 neurons had composite RFs covering more than one of five oral structures: lip, cheek mucosa, teeth/gingiva, tongue, and palate. The relative incidence of neurons with composite RFs was significantly higher in area 2 than in areas 3b and 1 (interstructural integration). These results indicate that the convergence of inputs from oral structures proceeds in a hierarchical manner across the postcentral gyrus, but chiefly in area 2 for the bimaxillary and interstructural integrations. The relative incidence of neurons with composite RFs was higher among neurons associated with the teeth/gingiva or palate than among neurons associated with the tongue or lip in all three areas. We interpret this to mean that anatomical or functional differences between oral structures might be reflected in the converging patterns in the oral representation.

Somatosensory association cortices

The somatosensory association cortices we refer to here are those areas in the caudal postcentral gyrus and in the frontoparietal operculum, the second somatosensory cortex. In a series of single unit studies in monkeys, we have demonstrated that the complexity of receptive field properties increases along the rostrocaudal axis of the postcentral gyrus, and proposed a hierarchical scheme for information processing in this gyrus. The hierarchical scheme has led us to find more complex types of somatosensory integration in the intraparietal region: integration of bilateral sides of the body, and that of somatosensory and visual information take place in the caudal-most part of the postcentral gyrus. Recent brain imaging studies in humans confirmed the presence of hierarchical processing in the postcentral gyrus. Also, studies in monkeys and those performed in human subjects have suggested that the caudal part of the postcentral gyrus is one of the key stations for perception of the peripersonal space and for the formation of body image. We further studied neuronal receptive field properties in the second somatosensory cortex (SII). There, neurons with bilateral receptive fields are in the majority. Hands and arms are dominant. Remote and discontinuous body regions were integrated in various combinations. These results support the notion that SII is a station higher than the postcentral regions.

Parallel pain processing in freely moving rats revealed by distributed neuron recording

The present study was designed to examine the possible differential roles of the medial and lateral pain systems in pain perception. We used a microwire array recording technique to record the pain-evoked neural activity of multiple neurons in freely moving rats. Noxious radiant heat was delivered to either hind-paw in a randomized order. A total of 256 single units were recorded in primary somatosensory cortex (SI), anterior cingulate cortex (ACC), and medial dorsal (MD) and ventral posterior (VP) thalamus during the painful stimulation. The results showed that SI neurons displayed a strong pain-related excitatory response with short duration and significant contralateral bias; VP had very similar functional patterns to that of SI. This suggested that SI, together with VP, participate in the processing of the sensory-discriminative aspect of pain. In contrast, ACC and MD shared common characteristics of moderate and longer-lasting increase of neural activity, bilateral receptive fields without contralateral preference, as well as the anticipatory response at the start of a painful stimulus, corresponding to the specific role of ACC and MD in the affective-motivational aspects of pain. The results provide an initial demonstration of distributed activity patterns within different pain systems in awake and freely moving rats, hence, providing confirmation of the existence of the dual pain pathways.

A review of contralateral responses to a unilateral inflammatory lesion.

Symmetry is a remarkably constant clinical feature of chronic inflammatory disease. Rheumatoid arthritis is almost by definition symmetrical [1]. Osteoarthritis, psoriasis and some of its associated arthritides are also symmetrical [2–4]. Pulmonary fibrosis, glomerulonephritis and sympathetic ophthalmia are also symmetrical inflammatory conditions. Whilst the pathophysiology behind this symmetry is unexplained, we and others have speculated that it is likely to be mediated via neurological mechanisms crossing through the spinal cord [5, 6]. The two sides of the spinal column have largely been thought to function independently of each other. There are three lines of evidence to suggest that this is not true. Careful anatomical studies of the spinal cord show transmedian fibres decussating posteriorly at all levels of the spinal cord to synapse in the laminae on the contralateral dorsal horn. These neuronal connections have been seen in many different species, including several primates (Fig. 1). Szentagothai [7], using Golgi analysis on young cats and dogs, showed that neurons with their cell bodies in the substantia gelatinosa send contralateral axons that appear to synapse in the contralateral substantia gelatinosa. Perl and Light [8] corroborated these findings after they had applied horseradish peroxidase to rat, cat and monkey dorsal rootlets. They found projections into the contralateral substantia gelatinosa as well as the ventral portion of the nucleus propius. Culberson et al. [9], using cresyl violet acetate (Fink-Heimer method), identified crossed afferent projections throughout the spinal cord, originating and terminating in laminae III–IV, in four mammalian species. These anatomical studies provide evidence that the opportunity exists for crosstalk between the left and the right sides of the spinal column. Functional studies of decerebrate rats demonstrate that such cross-communication can produce contralateral responses. Electrical stimulation of contralateral peripheral nerves is known to inhibit flexor reflex pathways in the spinal cord [10] as well as the long latency of C-fibre-evoked activity in dorsal horn cells [11, 12]. Contralateral dorsal horn cells are inhibited in response to noxious stimuli applied to the limb or tails of rats [13, 14]. Further electrophysiological studies confirm the presence of neurons in the dorsal horn that have bilateral receptive fields. Of relevance to this article is that the number of these neurons with bilateral receptive fields increases in the presence of unilateral inflammation [15, 16]. Grubb et al. [17] also showed that some of the fields on the contralateral side can become excitatory rather than inhibitory. At what level are these contralateral responses mediated? Woolf [16] documented the persistent reduction in flexor reflex thresholds contralaterally after noxious thermal stimuli had been applied to decerebrate rats with an intact brainstem. Fitzgerald [18], using a decerebrate, spinalized rat model, showed that a contralateral effect on dorsal horn fibres need not involve such higher pathways. Although direct contralateral spinal pathways exist in experimental conditions, there are likely to be significant supraspinal influences in vivo. This is suggested by several studies detailing an attenuation of central sensitization and secondary hyperalgesia following spinalization or inactivation of the rostral ventral medulla in a review of rat models of acute pain [19].

Hierarchical somesthetic processing of tongue inputs in the postcentral somatosensory cortex of conscious macaque monkeys.

The representation of the oral structures in the lateralmost part of the postcentral somatosensory cortex in conscious macaque monkeys was studied by recording the activities of single neurons. A total of 104 penetrations were made in the oral regions of six hemispheres in four animals and 2,292 neurons were isolated. The characteristics of the receptive fields (RF) of 1,598 neurons were identified. Of them, 513 neurons (area 3b, 196; area 1, 104; area 2, 213) along 44 penetrations responded to mechanical stimulation of the tongue (tongue neurons). The relative incidence of tongue neurons that had bilateral RFs increased gradually (bilateral integration) on moving caudally from area 3b to area 2. There was also a tendency for the RFs on the tongue to expand in the anteroposterior axis of the tongue (anteroposterior integration). Furthermore, the relative incidence of tongue neurons with composite RFs covering both the tongue and other surrounding oral structures was significantly higher in area 2 than in areas 3b and 1 (interstructural integration). As a result of the bilateral, anteroposterior and interstructural integration, the extent of the RFs of tongue neurons increased progressively from area 3b to area 2. We therefore concluded that hierarchical somatosensory processing, which has been established in the postcentral somatosensory cortex representing other body parts, is also present in the oral representation. We speculate that the hierarchical scheme in the oral representation might be a prerequisite neural process for the oral stereognosis that eventually takes place in the association cortices.

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.

Crossed and uncrossed projections to the cat sacrocaudal spinal cord: III. Axons expressing calcitonin gene-related peptide immunoreactivity.

We have investigated the projection patterns of peptidergic small-diameter primary afferent fibers to the cat sacrocaudal spinal cord, a region associated with midline structures of the lower urogenital system and of the tail. Calcitonin gene-related peptide (CGRP)-immunoreactive (CGRP-IR) primary afferent fibers were observed within the superficial laminae, rostrally as the typical inverted U-shaped band that capped the separate dorsal horns (S1 to rostral S2) and caudally as a broad band that spanned the entire mediolateral extent of the fused dorsal horns (caudal S2 and caudal). Within the dorsal gray commissure, labeling was seen as a periodic vertical, midline band. CGRP-IR labeling was prevalent in an extensive mediolateral distribution at the base of the dorsal horn, originating from both lateral and medial collateral bundles that extend from the superficial dorsal horn. Some bundles, in part traveling within the dorsal commissure, conspicuously crossed the midline. In addition to the robust projection to the superficial dorsal horn, there was a more extensive distribution of CGRP-IR fibers within the deeper portions of the cat sacrocaudal dorsal horn than has been reported for other regions of the cat spinal cord. Presumably, these deep projections convey visceral information to projection or segmental neurons at the neck of the dorsal horn and in the region of the central canal. This deep distribution overlaps the reported projections of the pelvic and pudendal nerves. In addition, the contralateral projections of CGRP-IR fibers may form an anatomical substrate of the bilateral receptive fields for selective dorsal horn neurons. The density and variety of CGRP-IR projection patterns is a reflection of the functional attributes of the innervated structures.