Response and receptive-field properties of spinomesencephalic tract cells in the cat

Recordings were made from 90 identified spinomesencephalic tract (SMT) cells in the lumbosacral spinal cord of cats anesthetized with alpha-chloralose and pentobarbital sodium. Recording sites were located in laminae I-VIII. Antidromic stimulation sites were located in different regions of the rostral and caudal midbrain including the periaqueductal gray, midbrain reticular formation, and the deep layers of the superior colliculus. Twelve SMT cells were antidromically activated from more than one midbrain level or from sites in the medial thalamus. The mean conduction velocity for the population of cells sampled was 45.2 +/- 21.4 m/s. Cells were categorized based on their responses to graded intensities of mechanical stimuli and the location of excitatory and/or inhibitory receptive fields. Four major categories of cells were encountered: wide dynamic range (WDR); high threshold (HT); deep/tap; and nonresponsive. WDR and HT cells had excitatory and/or inhibitory receptive fields restricted to the ipsilateral hindlimb or extending to other parts of the body including the tail, forelimbs, and face. Some cells had long afterdischarges following noxious stimulation, whereas others had high rates of background activity that was depressed by nonnoxious and noxious stimuli. Deep/tap cells received convergent input from muscle, joint, or visceral primary afferent fibers. The placement of mechanical lesions at different rostrocaudal levels of the cervical spinal cord provided information related to the spinal trajectory of SMT axons. Six axons were located contralateral to the recording electrode in the ventrolateral/medial or lateral funiculi while two were located in the ventrolateral funiculus of the ipsilateral spinal cord. Stimulation at sites used to antidromically activate SMT cells resulted in the inhibition of background and evoked responses for 22 of 25 cells tested. Inhibitory effects were observed on responses evoked by low/high intensity cutaneous stimuli and by the activation of joint or muscle primary afferent fibers. Based on the response and receptive-field properties of SMT cells it is suggested that the SMT may have an important role in somatosensory mechanisms, particularly those related to nociception.     

Response properties of whisker-associated trigeminothalamic neurons in rat nucleus principalis

Nucleus principalis (PrV) of the brain stem trigeminal complex mediates the processing and transfer of low-threshold mechanoreceptor input en route to the ventroposterior medial nucleus of the thalamus (VPM). In rats, this includes tactile information relayed from the large facial whiskers via primary afferent fibers originating in the trigeminal ganglion (NV). Here we describe the responses of antidromically identified VPM-projecting PrV neurons (n = 72) to controlled ramp-and-hold deflections of whiskers. For comparison, we also recorded the responses of 64 NV neurons under identical experimental and stimulus conditions. Both PrV and NV neurons responded transiently to stimulus onset (ON) and offset (OFF), and the majority of both populations also displayed sustained, or tonic, responses throughout the plateau phase of the stimulus (75% of NV cells and 93% of PrV cells). Average ON and OFF response magnitudes were similar between the two populations. In both NV and PrV, cells were highly sensitive to the direction of whisker deflection. Directional tuning was slightly but significantly greater in NV, suggesting that PrV neurons integrate inputs from NV cells differing in their preferred directions. Receptive fields of PrV neurons were typically dominated by a "principal" whisker (PW), whose evoked responses were on average threefold larger than those elicited by any given adjacent whisker (AW; n = 197). However, of the 65 PrV cells for which data from at least two AWs were obtained, most (89%) displayed statistically significant ON responses to deflections of one or more AWs. AW response latencies were 2.7 +/- 3.8 (SD) ms longer than those of their corresponding PWs, with an inner quartile latency difference of 1-4 ms (+/-25% of median). The range in latency differences suggests that some adjacent whisker responses arise within PrV itself, whereas others have a longer, multi-synaptic origin, possibly via the spinal trigeminal nucleus. Overall, our findings reveal that the stimulus features encoded by primary afferent neurons are reflected in the responses of VPM-projecting PrV neurons, and that significant convergence of information from multiple whiskers occurs at the first synaptic station in the whisker-to-barrel pathway.     

Response dynamics and receptive-field organization of catfish amacrine cells.

1. We have applied Wiener analysis to a study of response dynamics of N (sustained) and C (transient) amacrine cells. Stimuli were a spot and an annulus of light, the luminance of which was modulated by two independent white-noise signals. First- and second-order Wiener kernels were computed for each spot and annulus input. The analysis allowed us to separate a modulation response into its linear and nonlinear components, and into responses generated by a receptive-field center and its surround. 2. Organization of the receptive field of N amacrine cells consists of both linear and nonlinear components. The receptive field of linear components was center-surround concentric and opposite in polarity, whereas that of second-order nonlinear components was monotonic. 3. In NA (center-depolarizing) amacrine cells, the membrane DC potentials brought about by the mean luminance of a white-noise spot or a steady spot were depolarizations, whereas those brought about by the mean luminance of a white-noise annulus or a steady annulus were hyperpolarizations. In NB (center-hyperpolarizing) amacrine cells, this relationship was reversed. If both receptive-field center and surround were stimulated by a spot and annulus, membrane DC potentials became close to the dark level and the amplitude of modulation responses became larger. 4. The linear responses of a receptive-field center of an N amacrine cell, measured in terms of the first-order Wiener kernel, were facilitated if the surround was stimulated simultaneously. The amplitude of the kernel became larger, and its peak response time became shorter. The same facilitation occurred in the linear responses of a receptive-field surround if the center was stimulated simultaneously. 5. The second-order nonlinear responses were not usually generated in N amacrine cells if the stimulus was either a white-noise spot or a white-noise annulus alone. Significant second-order nonlinearity appeared if the other region of the receptive field was also stimulated. 6. Membrane DC potentials of C amacrine cells remained at the dark level with either a white-noise spot or a white-noise annulus. The cell responded only to modulations. 7. The major characteristics of center and surround responses of C amacrine cells could be approximated by second-order Wiener kernels of the same structure. The receptive field of second-order nonlinear components of C amacrine cells was monotonic.(ABSTRACT TRUNCATED AT 400 WORDS)     

Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex.

Receptive fields have been characterized independently in the lemniscal auditory thalamus and cortex, usually with spectrotemporally simple sounds tailored to a specific task. No studies have employed naturalistic stimuli to investigate the thalamocortical transformation in temporal, spectral, and aural domains simultaneously and under identical conditions. We recorded simultaneously in the ventral division of the medial geniculate body (MGBv) and in primary auditory cortex (AI) of the ketamine-anesthetized cat. Spectrotemporal receptive fields (STRFs) of single units (n = 387) were derived by reverse-correlation with a broadband and dynamically varying stimulus, the dynamic ripple. Spectral integration, as measured by excitatory bandwidth and spectral modulation preference, was similar across both stations (mean Q(1/e) thalamus = 5.8, cortex = 5.4; upper cutoff of spectral modulation transfer function, thalamus = 1.30 cycles/octave, cortex = 1.37 cycles/octave). Temporal modulation rates slowed by a factor of two from thalamus to cortex (mean preferred rate, thalamus = 32.4 Hz, cortex = 16.6 Hz; upper cutoff of temporal modulation transfer function, thalamus = 62.9 Hz, cortex = 37.4 Hz). We found no correlation between spectral and temporal integration properties, suggesting that the excitatory-inhibitory interactions underlying preference in each domain are largely independent. A small number of neurons in each station had highly asymmetric STRFs, evidence of frequency sweep selectivity, but the population showed no directional bias. Binaural preferences differed in their relative proportions, most notably an increased prevalence of excitatory contralateral-only cells in cortex (40%) versus thalamus (23%), indicating a reorganization of this parameter. By comparing simultaneously along multiple stimulus dimensions in both stations, these observations establish the global characteristics of the thalamocortical receptive field transformation.     

The topology of dermatomal projection in the medial lemniscal system

1. The topographic organization of first order afferent fibres in the lumbar, sacral and coccygeal dorsal roots, and in the fasciculus gracilis was studied in squirrel monkeys.2. At the entry zone, progressing from caudal to rostral, dorsal root filaments receive fibres from tail and hind-limb receptive fields which serially overlap and describe a spiral-shaped trajectory. The latter starts with tail, progresses post-axially towards the foot, crosses the foot from lateral to medial, and ascends the preaxial leg.3. In the fasciculus gracilis, this arrangement of fibres at the dorsal root entry zone is preserved in its entirety. It assumes the form of a fibre lamination, with the most caudal dorsal root fibres occupying a dorso-medial location; further rostral dorsal root fibres come to lie more ventrolaterally.4. Dorsum and sole of foot project in an overlapping and interdigitating manner to the fibre lamina of the 7th lumber dermatome in the fasciculus gracilis. Thereby, dorsum and sole of foot behave in the projection as if they were one and the same surface.5. The argument is presented that the foot and its projection on to the cross-sectional plane of the dorsal funiculus are topologically equivalent and that the hind-limb as a whole and its projection are not. On the other hand, homotopic mapping of the foot together with the sequential fibre organization in the dorsal funiculus enable many more types of closed curves on the body surface to remain arc-wise connected in the projection than would otherwise be possible.     

The cells of origin of the trigeminothalamic,trigeminospinal and trigeminocerebellar projections in the cat

Using the retrograde horseradish peroxidase technique, we have examined the distribution of labeled thalamic-, spinal- and cerebellar-projecting neurons in the trigeminal sensory nuclei of the cat.Injections into the nucleus ventralis posterior of the thalamus resulted in labeling of neurons in lamina I (subnucleus zonalis), the deeper part of lamina IV (the subhucleus magnocellularis) of the nucleus caudalis and in lamina V (the lateral extension of the nucleus medullae oblongatae centralis) on the contralateral side. A very large number of labeled small neurons were observed mainly in the caudal part of the nucleus interpolaris and in the ventral division of the principal sensory nucleus on the contralateral side and in the dorsal division of the principal sensory nucleus on the ipsilateral side.Injections into the known projection areas of the cerebellar cortex labeled mainly ipsilaterally the trigeminocerebellar neurons in a restricted ventrolateral area of lamina IV of the nucleus caudalis at its rostral level and in lamina V. Many labeled neurons were also observed in the nucleus interpolaris. Although the distribution overlapped with that of the trigeminothalamic neurons, the greatest majority were concentrated in its rostral part where the trigeminothalamic neurons were very small in number. In addition, labeled neurons were observed in the rostral part of the nucleus oralis and the ventralmost part of the ventral division of the principal sensory nucleus. No labeled neurons were observed in the dorsal division of the principal sensory nucleus and the mesencephalic nucleus.The trigeminospinal neurons were labeled mainly ipsilaterally following injections into the upper cervical cord. They were located in laminae I and III, the deeper part of lamina IV of the nucleus caudalis and in lamina V. Only scattered labeled neurons were found in the nucleus interpolaris. The number of labeled neurons increased in the nucleus oralis at the level of the superior olive. They tended to be distributed around or dorsal to the groups of the trigeminothalamic neurons at the caudal part of the principal sensory nucleus. No neurons of the principal sensory nucleus appeared to project to the spinal cord. Based on the large size and location, the trigeminospinal neurons could be differentiated from the other projection neurons in the nucleus oralis.The present study demonstrates that the trigeminal sensory nuclei are composed of groups of neurons with different projections, since the main aggregations are localized at different levels. However, it should be examined whether the neuronal groups, which are labeled from the different structures in similar locations, are composed of individual neurons projecting to more than one of these structures.     

Thermoreceptive lamina I trigeminothalamic neurons project to the nucleus submedius in the cat

Summary The technique of antidromic mapping with a roving array of electrodes was used to demonstrate that lamina I trigeminothalamic cells responsive specifically to skin temperature project to the n. submedius (Sm) in the medial thalamus of the cat. This finding indicates that Sm receives thermoreceptive in addition to nociceptive information.     

Modulation of lemniscal input during conditioned arm movements in the monkey

Summary Modulation of sensory transmission in the lemniscal system was investigated in 2 monkeys trained to perform a simple elbow flexion in response to an auditory cue. Evoked responses to peripheral stimulation were recorded in the medial lemniscus, sensory thalamus (ventral posterior lateral nucleus, caudal division, VPLc) and somatosensory cortex. Simultaneous recordings were made from the cortex and either the medial lemniscus or VPLc. At all recording sites, evoked responses to natural (air puff) or electrical, percutaneous stimulation were depressed prior to and during active movement. The time course of the depression was similar at all three levels; the magnitude of the decrease during movement was most pronounced at the cortical level. Cortical evoked responses to central stimulation of effective sites in either the medial lemniscus or VPLc were decreased during, but not before, the onset of movement. The decrease was less than that seen for peripheral evoked potentials. Passive movement of the forearm significantly decreased all but the lemniscal evoked potential. The results indicate that there is a centrally mediated suppression of somatosensory transmission prior to, and during movement, occurring at the level of the first relay, the dorsal column nuclei. During movement, reafferent signals from the moving arm decrease transmission at the thalamocortical level.     

Comparison of receptive-field organization of the superior colliculus in Siamese and normal cats

1. The superior colliculus has been studied in Siamese and normal cats by recording the responses of single tectal units to visual stimuli.

2. The retinotopic organization of the superior colliculus has been compared in the two breeds. In the normal cat, the contralateral half-field is represented in the central and caudal part of the colliculus, and a vertical strip of the ipsilateral half-field, 15-20° wide, is represented at the anterior tip. The Siamese cat superior colliculus receives an abnormally large projection from the ipsilateral half-field so that units with visual receptive fields which extend as far as 40° into the ipsilateral half-field can be found. The area of the tectal surface devoted to the representation of the ipsilateral half-field is about twice as large in Siamese cats as in normal cats. The enhanced representation of the ipsilateral half-field in Siamese cats is reflected in a displacement of the vertical meridian and the area centralis on the tectal surface.

3. The area centralis in the Siamese cat is located at about the same point on the tectal surface as would be occupied by a point in the visual field about 6-7° contralateral to the area centralis in the normal cat. The smallest receptive fields in both breeds are located near the area centralis. The size of the receptive field for a tectal unit seems to be determined by the retinal location of the receptive field and not by the absolute position of the unit on the tectal surface.

4. The receptive-field characteristics of tectal units show many similarities in the two breeds. The receptive fields of individual units consist of activating regions flanked by suppressive surrounds. Units respond well to stimuli of different shapes and orientation provided they are moving. The optimum stimulus for a given unit can be much smaller than the size of the activating region. About two thirds of the units studied in both breeds show directional selectivity. Most of the units studied in normal cats can be activated by stimulation of either eye, while in Siamese cats, 80% of the units studied can be driven only by the contralateral eye. A few monocularly driven units with two separated receptive fields have been observed in Siamese cats.

5. In the left tectum of both breeds, units respond well to left-to-right stimulus movement. The reverse situation obtains in the right tectum. In Siamese cats, units located at the anterior tip of the tectum with their receptive fields located in the visual half-field ipsilateral to the tectum under study respond better to stimulus movement toward the area centralis than away from it. The preferred direction for a tectal unit seems to be determined by its tectal location rather than by the location of its receptive field in the retina.

6. Visual cortex lesions in both breeds increase the responsiveness of tectal units to flashing spots and almost entirely remove the directional selectivity exhibited by tectal units, although units with asymmetric surrounds are still found. In normal cats, the lesions change the ocular dominance distribution, skewing it more strongly toward the contralateral eye. In Siamese cats, the ocular dominance distribution remains unchanged after a visual cortex lesion.

7. The squint commonly exhibited by Siamese cats is regarded as a compensation for the anomalous retinotectal topography. It is suggested that, in the absence of an adaptive modification, the anomalous retinotectal projection would lead to mislocalization in Siamese cats just as it does in frogs and hamsters whose retinotectal projection has been experimentally altered. The convergent strabismus which Siamese cats commonly exhibit may be a cure for the abnormal retinal projections rather than a disease.

     

Superior olivary and lateral lemniscal neurons projecting to the cochlea in the guinea pig

Efferent neurons to the cochlea in the guinea pig were observed in the superior olivary complex and ventral lateral lemniscal nuclei after injection of WGA-HRP into the cochlea via the round window. Of HRP-labeled nerve cells found in the brainstem, about 60% and 10% were located in the ipsilateral lateral superior olivary nucleus (LSO) and the contralateral ventral nucleus of the trapezoid body (VTB), respectively. A few labeled neurons were found in the ipsilateral VTB, contralateral LSO and the bilateral superior paraolivary nucleus (SPO). Seven percent and 5% of the labeled neurons were definitely observed in the ventrocaudal part of the contra- and ipsilateral ventral nucleus of the lateral lemniscus (VLL), respectively. A combination of acetylcholine esterase (AChE) histochemistry with the tracing of retrograde axonal transport of a fluorescent dye (DAPI) revealed that VLL neurons projecting to the cochlea, as well as about 85% of LSO neurons projecting to the ipsilateral cochlea, were AChE-positive.     

Differential projections of thermoreceptive and nociceptive lamina I trigeminothalamic and spinothalamic neurons in the cat

The projections of 40 trigeminothalamic or spinothalamic (TSTT) lamina I neurons were mapped using antidromic activation from a mobile electrode array in barbiturate anesthetized cats. Single units were identified as projection cells from the initial array position and characterized with natural cutaneous stimuli as nociceptive-specific (NS, n = 9), polymodal nociceptive (HPC, n = 8), or thermoreceptive-specific (COOL, n = 22; WARM, n = 1) cells. Thresholds for antidromic activation were measured from each electrode in the mediolateral array at vertical steps of 250 microm over a 7-mm dorsoventral extent in two to eight (median = 6.0) anteroposterior planes. Histological reconstructions showed that the maps encompassed all three of the main lamina I projection targets observed in prior anatomical work, i.e., the ventral aspect of the ventroposterior complex (vVP), the dorsomedial aspect of the ventroposterior medial nucleus (dmVPM), and the submedial nucleus (Sm). The antidromic activation foci were localized to these sites (and occasional projections to other sites were also observed, such as the parafascicular nucleus and zona incerta). The projections of thermoreceptive and nociceptive cells differed. The projections of the thermoreceptive-specific cells were 20/23 to dmVPM, 21/23 to vVP, and 17/23 to Sm, whereas the projections of the NS cells were 1/9 to dmVPM, 9/9 to vVP, and 9/9 to Sm and the projections of the HPC cells were 0/8 to dmVPM, 7/8 to vVP, and 6/8 to Sm. Thus nearly all thermoreceptive cells projected to dmVPM, but almost no nociceptive cells did. Further, thermoreceptive cells projected medially within vVP (including the basal ventral medial nucleus), while nociceptive cells projected both medially and more laterally, and the ascending axons of thermoreceptive cells were concentrated in the medial mesencephalon, while the axons of nociceptive cells ascended in the lateral mesencephalon. These findings provide evidence for anatomical differences between these physiological classes of lamina I cells, and they corroborate prior anatomical localization of the lamina I TSTT projection targets in the cat. These results support evidence indicating that the ventral aspect of the basal ventral medial nucleus is important for thermosensory behavior in cats, consistent with the view that this region is a primordial homologue of the posterior ventral medial nucleus in primates.     

Tactile discrimination study of the dorsal column-medial lemniscal system and spino-cervico-thalamic tract in cat

Summary The role of two spinal sensory pathways, the dorsal column (DC) pathway and the spino-cervico-thalamic tract (SCTT), involved in tactile discrimination was studied. Pour lesion groups of cats (DC lesion, SCTT lesion, combined DC and SCTT lesion, and sham-operated) were tested to discriminate various degrees of roughness. Animals with either the SCTT or the combined lesions performed at around 50–60% level under all the conditions tested. On the other hand, those with the DC lesion and sham-operations generally attained 80–100% level of performance.A difference between the DC group and sham-operated group was found in their rate of learning and ability for finer discrimination. These results are interpreted as an indication that a duplicity in transmission of tactile sensation exists, the DC pathway being more specific than the SCTT.This work was supported by USPHS Grants NB 00403, AM 6705 and FR 5384-07.     

Development of spatial receptive-field organization and orientation selectivity in kitten striate cortex

The functional organization of the receptive field of neurons in striate cortex of kittens from 8 days to 3 mo of age was studied by extracellular recordings. A quantitative dual-stimulus technique was used, which allowed for analysis of both enhancement and suppression zones in the receptive field. Furthermore the development of orientation selectivity was studied quantitatively in the same cells. Already in the youngest kittens the receptive fields were spatially organized like adult fields, with a central zone and adjacent flanks that responded in opposite manner to the light stimulus. The relative suppression in the subzones was as strong as in adult cells. Both simple and complex cells were found from 8 days. The receptive fields were like magnified adult fields. The width of the dominant discharge-field zone and the distance between the positions giving maximum discharge and maximum suppression decreased with age in the same proportions. The decrease could be explained by a corresponding decrease of the receptive-field-center size of retinal ganglion cells. Forty percent of the cells were orientation selective before 2 wk, and the fraction increased to 94% at 4 wk. Cells whose responses could be attenuated to at least half of the maximal response by changes of slit orientation were termed orientation selective. The half-width of the orientation-tuning curves narrowed during the first 5 wk, and this change was most marked in simple cells. The ability of the cells to discriminate between orientations in statistical terms was weak in the youngest kittens due to a large response variability, and showed a more pronounced development than the half-width did. The orientation-tuning curves were fitted by an exponential function, which showed the shape to be adultlike in all age groups. Two kittens were dark reared until recording at 1 mo of age. The spatial receptive-field organization and the orientation selectivity in these kittens were similar to normal-reared kittens at 1 mo. The responsivity of the cells of the dark-reared kittens was lower, and the latency before firing was longer than in the normal-reared kittens of the same age, and these response properties were more similar to those in 1- to 2-wk-old normal kittens. Our results indicate that the spatial organization of the receptive field is innate in most cells and that visual experience is unnecessary for the organization to be maintained and for the receptive-field width to mature during the first month postnatally.(ABSTRACT TRUNCATED AT 400 WORDS)