Innervation patterns of cutaneous hair receptors in cat

Cat hair receptors were studied to determine whether they could be distinguished by the following receptive field characteristics: thickness of innervated guard hairs, distance between innervated follicles and receptive field size. Initially the receptors were classified as G1, GI, G2 or D on the basis of their velocity requirements for excitation, their degree of linear directionality, their vibrational sensitivity, and whether they were activated by movement of down hairs. It was found that the thickest guard hairs on the posterior aspect of a cat's hindleg were usually 4-5 times thicker than the thinnest guard hairs from the same area and that G1, GI and G2 neurons innervated the full range of guard hair thicknesses available. Although there was a tendency for thicker guard hairs to be more heavily innervated, none of the neurons studied innervated thick guard hairs exclusively. While movement of the down hair and most guard hairs within D-mechanoreceptive fields easily evoked activity, a few guard hairs were regularly found for which mechanical displacement did not elicit a discharge even though they were well within the receptive field. Receptive field sizes and nearest neighbor distances between innervated follicles were smaller for D than for G1, GI and G2 receptors and greater for G1 than GI and G2 receptors.     

Descending influences on receptive fields and activity of single units recorded in laminae 1, 2 and 3 of cat spinal cord

Units (180) were isolated in laminae 1, 2 and 3 in segments L7-S1 of decerebrate cat spinal cord. For each unit, the size and nature of its receptive field (RF) was delineated. Then the dorsolateral funiculus (DLF) was stimulated for 1 sec with 10 or 50 Hz, 0.1 msec square waves and the response characteristics of the unit were again examined. Of the 108 units, 55 were excited or facilitated, 6 were inhibited (all in lamina 3) and 47 were unaffected. While some of the excited units responded only during the stimulus train, the majority showed prolonged excitation or facilitation lasting over one minute. The excited units were predominantly those responding to pressure or to brush, touch and pressure. Of the pressure units, 73% were excited or facilitated in contrast to only 29% of the brush/touch units. Most of the excited units showed expansion of their RFs.While many units of this type show ongoing variations of excitability and RF size, the evoked responses reported were sufficiently time-locked to the stimulus for it to be apparent that they were caused by the DLF stimulation. The units' responses still occurred when the DLF was stimulated caudal to a complete cord transection so that the effects did not pass through the brain stem.The major effect of descending systems or of DLF stimulation previously reported on the large cells of laminae 1, 4 and 5 has been inhibition. Here we report that a major descending influence on many units of laminae 1, 2 and 3 is excitatory. Therefore it is suggested that a population of small interneurons in the superficial laminae could contribute to the descending inhibition of large dorsal horn neurons.     

Somatotopic component of the multisensory map in the deep laminae of the cat superior colliculus.

The topographic organization of the somatosensory representation in the deep layers of the cat superior colliculus was reexamined using methods previously used to examine the visuotopy in these layers. This technique identified the distribution of neurons in the superior colliculus that represent a designated region of the body surface (i.e., a dermal image), as well as assessed the differential distribution of deep layer neurons representing different body regions (e.g., face, forelimb, hindlimb, etc.). When the area of densest representation within a dermal image was considered, a well-ordered somatotopy was evident that was similar to the one previously described (Stein et al., '76: J. Neurophysiol. 39:401-419). Each region of the body surface, however, was represented within a surprisingly broad area of the deep layers, which often had considerable overlap with the representations of adjacent body regions. This organization was similar to that of the deep layer visuotopy and emphasizes that the representation of a peripheral stimulus is accomplished by the simultaneous activation of a large population of deep layer neurons. Furthermore, an examination of the convergence patterns on somatosensory-responsive neurons demonstrated that the somatotopy was formed primarily by multisensory neurons. These data indicate that the somatosensory representation is best considered as a component of a comprehensive multisensory functional unit that plays a critical role in effecting behavioral responses to a wide variety of stimuli.     

Lack of binocular activation of cells in area 19 of the Siamese cat

Single cells were recorded in area 19 of 8 Siamese cats. Receptive fields (RFs) were typical for this area in terms of size, directional specificity and type. However, 69 out of the 70 units found were monocularly driven through the contralateral eye. Moreover, the amount of excursion of RFs into the ipsilateral visual field was more limited than that generally demonstrated for areas 17 and 18, extending to a maximum of 5° with very few cells having RFs situated completely within the ipsilateral hemifield.     

Visual response properties of ventral lateral geniculate nucleus cells projecting to the pretectum and superior colliculus in the cat

The visual properties of cells in the cat ventral lateral geniculate nucleus (LGV) identified antidromically from the pretectum and/or superior colliculus (projection cells) were studied in comparison with those of LGV neurons which could not be activated antidromically (non-projection cells). ON-phasic receptive fields (RFs) were relatively predominant in 27 projection cells, whereas ON-tonic RFs were found more commonly in the non-projection group. The distribution of the RF centers revealed a centroperipheral gradient of the visual field representation within the LGV that the central visual field was more densely organized.     

The contralateral input to the dorsal horn of the spinal cord in the decerebrate spinal rat

Input from the contralateral limb and tail was examined in the lumbar dorsal horn of decerebrate spinal rats. Fifty-three cells were recorded from laminae 4, 5 and 6 and classified according to their ipsilateral response to natural and electrical stimulation. Twenty-nine (54%) of these cells were found to have inhibitory contralateral fields. This inhibition was evoked by noxious pinching or heating of the skin. In most cases the inhibitory field was a mirror image of the excitatory ipsilateral field although it also often included the tail. Activity evoked by natural and electrical stimulation as well as spontaneous activity was inhibited by contralateral skin stimulation. Noxious specific and wide dynamic range cells displayed these fields but low threshold mechanoreceptive cells did not. Twenty-six cells (49%) received direct short-latency excitatory input from the contralateral sciatic nerve; this correlated well with the presence of contralateral fields. Trains of stimuli applied to the contralateral sciatic nerve at Aδ- and C-fibre strength resulted in inhibition of the cell whereas trains of Aβ strength had no effect. The results demonstrate the existence of segmental contralateral control over dorsal horn cell activity, not involving supraspinal pathways.     

Immunocytochemical identification of serotonin axonal contacts on characterized neurons in laminae I and II of the cat dorsal horn

Serotonergic pathways from brainstem to spinal cord play an important role in the modulation of pain perception. To establish where that modulation occurs, we examined serotonin-immunoreactive axonal contacts on individually characterized laminae I and II dorsal horn neurons intracellularly filled with horseradish peroxidase. We found serotonin axonal contacts on marginal, stalked, and islet cells. Contacts preferentially occurred on dendritic shafts rather than on spines. Marginal and stalked cells received the heaviest innervation.     

Receptive field structure of area 19 as compared to area 17 of the cat

A total of 139 cells from area 19 along with a comparison sample of 172 cells from area 17 were classified using a system proposed by Orban and Kennedy, following Henry and consisting of 4 basic cell ‘families’, namely S,C,A and B, each having an end-stopped member: HS, HC, HA and HB. The two basic parameters separating the 4 families are firstly spatial overlap of ON and OFF subregions and secondly receptive field (RF) width. Spatial overlap was studied quantitatively in a number of these cells using multiple presentations of stationary slits or moving light and dark edges. RF width was determined quantitatively using bars moving at different velocities across the RF.It was found that cells with spatially nonoverlapping and overlapping subregions are present in both areas. S and HS cells, which shows similarities with simple cells, were encountered in area 19 but they constituted only 18% of the population as opposed to 55% in area 17. C and HC cells, reminiscent of complex cells, were about as common in area 19 as in area 17. In both areas C cells were the only group which consistently discharged equally well or better in response to diffuse light turned on and off than when presented with light bars. A and B families formed a minority in both areas. Area 19 contained a larger proportion of nonoriented and undriveable units, as well as a special category of cells preferring stimuli with a width larger than the length (‘rectangle cells’).RF width was generally larger in area 19 than in area 17 and its distribution in area 19 showed distinct peaks. In the part of area 19 subserving central vision these peaks appeared with a periodicity of 0.8°, suggesting that cells in this zone are supplied by one or more rows of a uniform set of afferents having a RF cetner diameter of about 0.8°. The identification of this population as W-relay cells is supported by the long latencies found in cells from this part of area 19.It is concluded that the basic principles underlying the structure of the RF are similar in both areas 19 and 17.     

Excitability and functional organization of cutaneous tactile units of the bullfrog (R. catesbeiana).

Frog skin touch receptors are discrete structures which appear as dome-shaped translucent elevations of the epidermis. These domes are particularly responsive to direct touch. Tactile stimulation of adjacent skin never caused impulse activity, except when the skin distortion disturbed the domes. On stimulation at threshold intensity, the response of all units studied always consisted of a single impulse whether the stimulus energy was electrical or mechanical. While most tactile units discharged one impulse upon application of mechanical stimulation, a few also discharged one impulse upon stimulus release (on-off response). No after discharge was seen at stimulus strengths of three or four times threshold or after repetitive stimulation at 1,000 pps. The range of distribution of active domes/receptive field was 1--14. Generally the most sensitive domes appeared to be in or near center field. Twice as many of the tactile units responded more readily to cold than to warmth. The impulse frequency of units responding to thermal stimulation ranged from 3-11/sec. The conduction velocity of tactile units measured was within a range of 9--25 m/sec, with a mean of 12 m/sec. The results suggest that the following: 1) the existence of discrete structures which respond to tactile stimuli; a phylogenetic relationship might be postulated; 2) cold/touch receptors which appear to be present in greater quantity in the frog's skin than are warm/touch receptors, 3) touch units which should be considered primarily as mechanoreceptors with a possible secondary function as thermoreceptors.     

The Classification and Properties of Nociceptive Afferent Units from the Skin of the Anaesthetized Pig

The afferent properties of nerve fibres innervating the hairy skin of the pig hind limb were investigated by recording from 142 single units from the saphenous nerve. Identified single units were isolated using maximal electrical stimulation of the nerve trunk. Afferent units were classified on the basis of their responses to a range of stimuli, both thermal (heating to 60°C and cooling to 10°C) and mechanical (air jet, von Frey type filaments with forces of 0.1–250 mN, and strong pressure with a blunt needle). A-fibre units (conduction velocity 6.3–64 m/s, n= 60) fell into categories that have been described in hairy skin in other mammalian species. Most were mechanoreceptors, although seven typical A-fibre mechanical nociceptors with large, multipoint fields were also isolated. No cutaneous receptive field could be found for 15% of A-fibre units. Out of 62 C-fibre units (conduction velocity 0.49–2 m/s) 40% had no cutaneous field for pressure, heat or cold. Of the C-fibre units with cutaneous fields, 42% were polymodal nociceptors, 38% were mechanoreceptors with a variety of properties, including some excited by noxious heat, and 19% were heat-only nociceptors. C-polymodal nociceptors had large receptive fields up to 12.5 mm across and did not sensitize following strong heating. Twenty units conducted at 2–6.3 m/s, between the main C- and A-fibre bands, and were varied in their responses. Some had properties identical to C-fibre mechanoreceptors whilst four were sensitive cold thermoreceptors and one was a polymodal nociceptor. Two units were mechanical nociceptors with small receptive fields. The innervation of pig skin thus has some features like that of primates, such as the presence of C-heat nociceptors and the large receptive fields of C-polymodal nociceptors. However, other features were like non-primates (e.g. the minimal heat-sensitivity of A-mechanical nociceptors) or were unique (the heat-sensitive mechanoreceptors and the lack of heat sensitization in C-polymodal nociceptors from hairy skin).     

Alterations in the ipsi- and contralateral afferent inputs of dorsal horn cells produced by capsaicin treatment of one sciatic nerve in the rat

Dorsal horn cells in the lumbar spinal cord of decerebrate spinal rats were examined 7-21 days following local application of capsaicin to the sciatic nerve. Such local capsaicin treatment is known not to influence the size of the incoming A and C fibre afferent volley. The receptive field properties and primary afferent input of cells on both sides of the cord, that is ipsi and contralateral to the treated nerve, were examined. On the treated side, the percentage of cells excited by C fibres from the capsaicin treated nerve was 30% of normal and the number of cells responding to noxious heating of the cutaneous receptive field was reduced by 50%. A fibre input and low and high threshold mechanical input were normal. The receptive field size was larger in many cells innervated by the treated nerve. On the side opposite to the treated nerve, responses to noxious and non-noxious stimulation of the untreated limb were unaffected as was the input from the untreated sciatic nerve. Receptive fields were somewhat larger than normal. Effects were also observed from contralateral stimuli. Cells on both sides of the cord were found with excitatory contralateral receptive fields and excitatory responses to trains of high intensity stimulation to the contralateral sciatic nerve. In untreated animals the effect of such contralateral stimulation is inhibitory. The results show that peripheral nerve capsaicin treatment causes long lasting reduction of the C fibre input to dorsal horn cells on the treated side. However, it also results in changes in the inhibitory and excitatory receptive fields of cells on both sides of the cord.     

Fractured cutaneous projections to the granule cell layer of the posterior cerebellar hemisphere of the domestic cat

Snider's pioneering studies of tactile responses in the cerebellar cortex of cats and monkeys suggested that posterior regions of the cerebellar hemispheres receive somatotopically organized projections. However, recent studies in rats, using high-density, in depth microelectrode mapping methods, have shown that tactile projections to the granule cell layer of the cerebellar hemispheres are somatotopically disrupted. We reexamined the Organization of cutaneous projections to eortibellar hemispheric cortex in cats by using micromapping methods. Natural stimulation of cutaneous surfaces evokes short-latency (mossy-fiber-induced) multiple unit responses in the cerebellar granule cell layer of crus II and paramedian lobule in both ketamine- and barbiturate-anesthetized cats. Facial structures are represented in several of the most caudo-medial folia of crus II as well as in three of the rostral folia of the paramedian lobule. In several of these paramedian folia, facial projections are interspersed with projections from the forelimb. Forelimb structures alone are represented in two intermediate folia of the paramedian lobule. No cutaneous projections were found from the trunk or hindlimb. All projections were from ipsilateral receptive fields. In four folia of crus II and six folia of the paramedian lobule, cutaneous projections form a mosaic of patchlike projections. Within single patches, projections are somatotopically organized, but projections to adjacent patches come from noncontiguous body regions. Within a single folium, a particular facial region may be represented in two or three spatially separated patches. Facial patches are small, usually less than 1 mm². Forelimb patches are usually larger, often extending the full length and breadth of a folial crown. Patches with like receptive fields are not organized in zonal sagittal strips. Rather than being somatotopically organized, cutaneous mossy fiber projections to granule cells in cats, as in rats, reveal a more complex mosaic pattern of organization.     

Changes in visual response properties of cat retinal ganglion cells within two weeks after axotomy

After optic nerve transection beta cells of cat retinal ganglion cells (RGCs) suffer from rapid cell death from 3 to 7 days, whereas alpha cells gradual cell death until 14 days. Here we report electrophysiological properties of Y- (morphological alpha) and X- (morphological beta) cells at 5 and 14 days after axotomy in comparison with those of intact Y- and X-cells. Most of the axotomized RGCs revealed characteristic visual response properties that enable us to classify them into Y- or X-cells. Physiological sampling ratio of X-cells sharply decreased from day 5 to 14 after axotomy, corresponding to the previous morphological results. As compared with intact RGCs, axotomized RGCs of both Y- and X-type revealed the following abnormalities: smaller receptive field centers, weaker visual responses and lower spontaneous activities. Intracellular injections of Lucifer yellow into axotomized and intact RGCs at eccentricities 0-6 mm from the area centralis revealed no sign of shrinkage in dendritic field size of either alpha or beta cells on day 5 and day 14 after axotomy, revealing that observed smaller receptive field centers of axotomized RGCs on day 5 were not due to the change of dendritic field sizes. These results suggest that the major events occurring shortly after axotomy are significant loss of synaptic inputs from afferent neurons in the retina and/or changes of membrane properties of axotomized RGCs. These events can also explain lower spontaneous activities and weaker visual responses of axotomized RGCs.     

Effects of 4-aminopyridine, GABA and bicuculline on cutaneous receptive fields of cat dorsal horn neurons

4-Aminopyridine (4-AP), bicuculline and GABA were applied locally to dorsal horn cells in the lumbar spinal cord in Nembutal-anaesthetized cats and in spinal cats. 4-AP expanded the cutaneous receptive field of 29 of 33 cells tested. Bicuculline and GABA had little or no effect on receptive field size.     

The effects of strychnine and bicuculline on the responses of X- and Y-cells of the isolated eye-cup preparation of the cat

The effects of strychnine and bicuculline, the respective antagonists of glycine and GABA, on the inhibitory responses of X- and Y-type retinal ganglion cells of the cat were investigated using an isolated eye-cup preparation. The surround inhibition of the on-center X-cell was blocked by strychnine, whereas that of the on-center Y-cell was blocked by bicuculline. In the case of the off-center cells, bicuculline indifferently blocked the center and the surround responses of either the X-cell or the Y-cell, but strychnine did not.     

Surround suppression sharpens orientation tuning in the cat primary visual cortex

In the primary visual cortex (V1), the response of a neuron to stimulation of its classical receptive field (CRF) is suppressed by concurrent stimulation of the extraclassical receptive field (ECRF), a phenomenon termed 'surround suppression'. It is also known that the orientation tuning of V1 neurons becomes sharper as the size of the stimulus increases beyond the CRF. However, there have been few quantitative investigations of the relationship between sharpening of orientation tuning and surround suppression. We examined this relationship in 73 V1 neurons recorded from anesthetized and paralysed cats using sinusoidal grating patches as stimuli. We found that sharpening of orientation tuning was significantly correlated with the strength of surround suppression for large stimuli that cover both CRF and ECRF. Furthermore, simulation analysis using a variety of tuning widths and most suppressive orientation of orientation-tuned surround suppression demonstrated that broadly orientation-tuned surround suppression sharpens orientation tuning for large gratings without shift in optimal orientation. Our findings suggest that one of the functional roles of surround suppression in V1 is enhancement of orientation discrimination for large and uniformly patterned objects.     

White noise analysis of cortical directional selectivity in cat

We studied spatiotemporal interactions in cat cortical receptive fields by presenting a stimulus composed of 16 narrow bars whose luminances were randomly modulated. Conventional stimuli were also presented to classify receptive field properties. A white noise estimate of the cell's response to a stepwise moving bar stimulus was calculated from responses to the spatiotemporal random stimulus. The white noise estimate captured the most important feature of the receptive field demonstrated by conventional stimuli, i.e. directional selectivity. In addition, the white noise analysis; (1) made visible inhibitory response phases that are usually below threshold; (2) subdivided the response into its linear and non-linear estimates; (3) further subdivided the non-linear estimate into spatial and temporal interactions; and (4) allowed estimation of responses to stimuli that were never explicitly presented.     

The ventral lateral geniculate nucleus in the cat: thalamic and commissural connections revealed by the use of WGA-HRP transport

The present investigation was carried out to clarify the topographical details of both the origin and terminal site of the thalamic projections and the commissural connections of the ventral lateral geniculate nucleus (LGNv) in the cat by using bidirectional transport of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP). Thalamic projections: Unilateral injections of WGA-HRP into the LGNv produced orthograde labeling in the intralaminar nuclei bilaterally and in the lateralis posterior (LP) and the pulvinar (Pul) nucleus ipsilaterally. In the intralaminar nuclei the rostral part of the nucleus centralis lateralis (CL) was most densely labeled by orthogradely transported material, particularly in its dorsal and lateral large-celled portion. Other intralaminar nuclei--such as the nucleus paracentralis, centralis medialis, and centralis dorsalis--also were labeled bilaterally with ipsilateral predominance, but no labeling was detected in the caudal portion of the CL and the centromedian and parafascicular nuclei. In the Pul, labeling of terminal ramifications was found to be concentrated in a region just medial to the so-called retinorecipient zone of the Pul as a slim band of labeling inclining dorsoventrally. In the LP, fine labeled fibers were located in the lateral portion of the LP. Commissural connections: Commissural fibers crossed in the dorsal part of the posterior commissure and reached the most caudal part of the contralateral LGNv. Labeling in the contralateral LGNv was concentrated in the dorsomedial part of the medial zone that extends medially to the middle portion of the cerebral peduncle. Origins of the commissural connections arose mostly from the medial zone that roughly corresponds to the commissural terminal zone and partly from aberrant cells dispersed among optic tract fibers. From these results, together with the previous studies, it is concluded that although the cat's LGNv has connections with diverse structures in the central nervous system, the origin and terminal site of the connections are partially segregated within the nucleus, which suggests that the LGNv may contain functional subsystems.     

The cutaneous contribution to the hamstring flexor reflex in the rat: an electrophysiological and anatomical study

The location and properties of the cutaneous receptive fields responsible for detecting the flexor withdrawal reflex in the posterior head of biceps femoris (pBF) and semitendinosus (ST) components of the hamstring muscle have been examined in unanaesthetized decerebrate rats, spinalized at T10-T11. Single alpha-motoneurone efferents were recorded from the nerve to pBF and the principal head of ST and their responses to ipsi- and contralateral hindlimb skin stimulation investigated. The efferents to both muscles characteristically had a low or absent background discharge and they all had mechanoreceptive fields on the ipsilateral foot. The mechanical threshold of these fields was high with no response to light touch or brush. Fifty-four percent of these units also had a smaller and weaker contralateral mechanoreceptive field. The only apparent difference between ST and pBF efferents was that more ST efferents had contralateral fields than pBF units. Noxious, hot and cold thermal stimuli applied to the ipsilateral foot activated 56% of the efferents. Mustard oil, a chemical irritant, produced a long-lasting flexor response when applied to the ipsilateral foot. The responses of these efferents to stimulation of A beta, A delta and C cutaneous afferents in the sural nerve were also studied. Short latency reflexes were elicited in all efferents by A beta inputs, longer latency reflexes were elicited in 64% by A delta inputs and very long latency responses with long afterdischarges were found in 73% of the units to C inputs. Retrograde labelling of the hamstring motoneurones with WGA-HRP indicated that they lay in ventrolateral lamina IX extending from the caudal portion of the third lumbar segment to the junction of the 5th and 6th lumbar segments. Transganglionic labelling of small diameter primary afferent terminals in the dorsal horn of cutaneous nerves innervating the foot revealed that the longitudinal distribution corresponded closely with that of the hamstring motor nucleus. The flex-or reflex in the spinal rat provides a useful model therefore, for studying how the input in nociceptive afferents is processed and transformed within the spinal cord, to produce appropriate outputs.