Richard M. Vickery

Synaptic transmission between single slowly adapting type I fibres and their cuneate target neurones in cat.

1. The synaptic linkage between single, identified slowly adapting type I (SAI) fibres and their central target neurones of the cuneate nucleus was examined in pentobarbitone‐anaesthetized cats. Simultaneous extracellular recordings were made from individual cuneate neurones and from fine, intact fascicles of the lateral branch of the superficial radial nerve in which it was possible to identify and monitor the activity of each group II fibre. Individual SAI fibres were activated by static displacement and by vibration delivered with a fine probe (0.25‐2 mm diameter) to their associated touch domes in the hairy skin of the forelimb. 2. Transmission properties across the synapse were analysed for nine SAI‐cuneate pairs in which the single SAI fibre of each pair provided a suprathreshold input to the cuneate neurone. Neither spatial nor temporal summation was required for effective impulse transmission, and often more than 80% of SAI impulses led to a response in the cuneate neurone. Responses of the cuneate neurones to single SAI impulses occurred at a short, fixed latency (S.D. often < 0.1 ms), and frequently consisted of a burst of two or three impulses, at low SAI input rates in particular. 3. The tight phase‐locking in the responses to vibration of single SAI fibres was preserved in the cuneate responses for frequencies up to approximately 400 Hz. However, as the impulse rates of the cuneate neurones were less than 150 impulses s‐1, their impulse patterns could not directly signal the vibration periodicity at frequencies > 100‐150 Hz despite 1:1 responses in their single SAI input fibres up to approximately 500 Hz. 4. The reliable transmission of touch dome‐associated SAI input across the cuneate nucleus indicates that transmission failure at this first relay is unlikely to be responsible for the reported failure of touch dome‐SAI inputs to contribute to tactile perception. 5. The transmission characteristics for the SAI fibres were very similar to those demonstrated previously for fibres associated with Pacinian corpuscles, which argues against any marked differential specialization in transmission characteristics for dorsal column nuclei neurones that receive input from different tactile fibre classes.

Spatial and temporal frequency selectivity of cells in area 21a of the cat.

1 The spatial and temporal response properties of single cells in area 21a of the anaesthetized cat were assessed using drifting sinusoidal gratings presented at the optimum orientation for each cell. 2 Responses to sinusoidal gratings were dominated by an elevation of the mean discharge, with a relatively small modulated component at the temporal frequency of grating drift. The relative modulation ratio for the majority of cells was less than 1, similar to complex cells in the striate cortex. 3 Of those cells responsive to stimulation with sinusoidal gratings, 94% displayed spatial bandpass characteristics. Values derived from spatial frequency tuning curves were: mean optimum spatial frequency, 0.26 cycles deg−1; mean spatial resolution, 0.86 cycles deg−1; mean spatial bandwidth, 1.8 octaves; and mean normalized bandwidth, 1.3. Two cells (6%) displayed spatial low‐pass characteristics. 4 Approximately half our sample of cells (44%) displayed temporal low‐pass tuning, while 35% displayed temporal bandpass characteristics. The mean optimum temporal frequency of bandpass cells was 3.3 Hz and the mean temporal bandwidth 1.9 octaves. The remaining cells were classified as temporal broadband (17%) and temporal high‐pass (4%). 5 We conclude that the dominant functional input to cells with relatively high spatial frequency selectivity and/or temporal low‐pass response properties most probably arises from area 17. The responses of the remaining cells may be explained by input from area 17 or 18.

Transmission characteristics for the 1:1 linkage between slowly adapting type II fibers and their cuneate target neurons in cat

Transmission from single, identified, slowly adapting type II (SAII) tactile fibers to their target neurons in the cuneate nucleus was examined in anesthetized cats. Simultaneous recordings were made from cuneate neurons and from fine, intact fascicles of the superficial radial nerve in which it was possible to identify and monitor the activity of each group II fiber. Selective activation of individual SAII fibers was achieved by means of skin stimulation with fine probes, in conjunction with extensive forelimb denervation. Responses were studied for seven SAII-driven cuneate neurons. For three there was unequivocal monitoring of the identified SAII input fiber. However, in six of the seven there was evidence that just one SAII fiber provided suprathreshold input to the cuneate neuron, and neither temporal nor spatial summation was required for reliable transmission. Cuneate impulse rates, in response to SAII inputs lasting 1 s, were less than 250 impulses per second, even though the SAII impulse rates could be 500 s-1. Responses to individual SAII impulses consisted of a burst of 2–3 impulses at low SAII input rates, but burst responses disappeared at high SAII rates. In all three SAII-cuneate pairs studied, the transmission security (the percentage of SAII impulses that evoked cuneate spike output) exceeded 80% in response to static skin displacement and in response to certain frequencies of skin vibration, in particular, at 100–200 Hz, exceeded 98% when the SAII fiber responded near the 1∶1 level (one impulse per vibration cycle). Transmission characteristics for the SAII-cuneate linkage resulted in the cuneate neuron showing tight phaselocking of responses to high-frequency (>100 Hz) vibrotactile stimuli and higher impulse rates than its SAII input (up to input rates of ∼50 impulses s-1). Security of transmission across the SAII-cuneate synapse is similar to that demonstrated previously for tactile fibers of the SAI and Pacinian corpuscle (PC)-related classes, which suggests that there is no marked differential specialization in transmission characteristics for dorsal column nuclei neurons that receive input from different tactile fiber classes. Furthermore, it means that the reported failure of individual SAII fiber inputs to generate conscious sensation in man following intraneural microstimulation is not related to transmission failure at the first central relay.

A patch-clamp investigation of membrane currents in a novel mammalian retinal ganglion cell line

We characterised membrane currents in undifferentiated RGC-5 cells, a cell line used in in vitro models of apoptosis and glaucoma. The cells were inexcitable, with no voltage-dependent Na(+) currents or action potentials. Some novel currents were observed including basal Cl(-) currents, inwardly rectifiying K(+) currents and Gd(3+) insensitive stretch-activated currents. Our results highlight the differences between the electrophysiological properties of undifferentiated RGC-5 cells and retinal ganglion cells.

Vibrotactile sensitivity of slowly adapting type I sensory fibres associated with touch domes in cat hairy skin.

1. Recordings were made from single slowly adapting type I (SAI) afferent fibres associated with touch domes in the cat hairy skin. Controlled vibratory stimuli were used first, to characterize the precision with which these SAI afferents reflect the temporal aspects of vibrotactile stimuli, and second, to determine whether earlier disparate reports of SAI responsiveness to vibration may be attributable to highly specific stimulus requirements. 2. Eighteen SAI fibres from femoral cutaneous nerve branches were examined; each was associated with one to three touch domes. SAI responses to both steps and sinusoidal vibration (1‐1.5 s in duration) were affected profoundly by both probe size and position. Punctate stimulus probes (250 microns) produced much higher response levels and steeper stimulus‐response relations than those elicited with large (2 mm) probes, probably on account of focal distortion created within the dome by the smaller probes. SAI sensitivity to vibration was also affected markedly by the amplitude of any pre‐indentation on which the vibration was superimposed; sensitivity was much lower when the pre‐indentation exceeded 100 microns, in particular with larger stimulus probes. 3. Measures of both vibration sensitivity and the precision of impulse patterning demonstrated that, if appropriate stimulus parameters are chosen, the SAI fibres can respond to 1 s trains of vibration (amplitude < or = 100 microns) in a tightly phase‐locked, 1:1 manner for frequencies up to 500 Hz. At frequencies from approximately 100‐500 Hz the SAI fibres displayed broad 1:1 plateaus, where their response rate remained constant over a range of amplitudes, and phased‐locking was tightest. Responses remained phase‐locked up to 1000 Hz, but could not follow the vibration with a 1:1 pattern above 500 Hz. 4. The results demonstrate that with appropriate stimulus parameters, touch dome‐associated SAI fibres are capable of signalling vibrotactile information over a similar bandwidth of frequencies as do Pacinian sensory fibres. The variability in past reports of SAI vibration sensitivity may relate principally to differences in stimulus conditions. However, in view of the SAI capacity for responding to vibration with temporally precise, patterned activity, it appears that their reported failure to contribute to vibrotactile sensibility must be attributed to limitations imposed in the central processing of SAI signals.

Responses of cat ventroposterolateral thalamic neurons to vibrotactile stimulation of forelimb footpads

SummaryResponses of neurons in the ventroposterolateral nucleus of the thalamus to vibration applied to the forelimb footpads were analyzed in anesthetized cats in order to describe the signalling properties of thalamic neurons that received input from the different classes of tactile afferents innervating the glabrous skin of the distal forelimb. Seventy-six thalamic neurons, the majority of which (60 of 76) were positively identified as thalamocortical projection neurons, were classified into two broad groups according to their responses to 1-s step indentations of the skin. A minority (24%) comprised neurons that had slowly adapting (SA) responses, whereas the remainder (76%), the dynamically sensitive neurons, had transient responses to the onset and offset phase of the step and were further classified according to their sensitivity to cutaneous vibrotactile stimuli into those activated by low-frequency vibration (rapidly adapting, RA, neurons) and those activated by high frequencies (Pacinian afferent, PC, neurons). Thalamic RA neurons displayed phaselocked responses to vibration at frequencies up to ∼100 Hz, while PC neurons displayed phaselocked responses to vibration up to 400–500 Hz. Thalamic SA neurons varied in their responses to vibrotactile stimuli; half were most sensitive to vibration frquencies of 50 Hz or less, while the others responded over a broader range of frequencies. Although three major classes of footpad-related thalamic neurons were identified, there was evidence of convergent input to a small proportion of them. The study demonstrates that thalamic neurons have the capacity for responding to cutaneous vibration with phaselocked, patterned impulse trains, which would enable them to encode information about vibrotactile frequencies up to ∼ 300 Hz.

Suppression of vibrotactile discrimination by transcranial magnetic stimulation of primary somatosensory cortex

A number of human and animal studies have reported a differential representation of the frequency of vibrotactile stimuli in the somatosensory cortices: neurons in the primary somatosensory cortex (SI) are predominantly responsive to lower frequencies of tactile vibration, and those in the secondary somatosensory cortex (SII) are predominantly responsive to higher frequencies. We employed transcranial magnetic stimulation (TMS) over SI in human subjects to investigate the extent to which the inactivation of SI disrupted the discrimination of vibrotactile stimulation at frequencies that give rise to the tactile sensations of flutter (30 Hz) and vibration (200 Hz). Frequency discrimination around the 30‐Hz standard following application of TMS to SI was reduced in seven of the eight subjects, and around the 200‐Hz standard was reduced in all eight subjects. The average change in discrimination following TMS was about 20% for both low and high frequencies of vibrotactile stimulation. These data suggest that disruption of SI: (1) has a direct effect on the discrimination of both low and high frequencies of vibrotactile stimuli, consistent with a serial model of processing, or (2) has a direct effect on low‐frequency vibrotactile stimuli and an indirect effect on the processing of high‐frequency vibrotactile stimuli by SII via cortico‐cortical connections between the two regions.

Responses of slowly adapting type II afferent fibres in cat hairy skin to vibrotactile stimuli.

1. Slowly adapting type II (SAII) afferent fibres that supply the forelimb were isolated from the medial cutaneous nerve of anaesthetized cats and examined for their capacity to signal information about vibrotactile events in the hairy skin. 2. The SAII fibres had a single spot‐like receptive field focus where they were highly sensitive to steady indentation and vibration applied with probes normal to the skin surface. However, their sensitivity was affected profoundly by the size of the stimulus probe, its position in relation to the receptive field focus and, to a lesser extent, the magnitude of any pre‐indentation on which vibration was superimposed. Small stimulus probes (e.g. 250 microns diameter) were much more effective than larger (> or = 1‐2 mm) ones, and small shifts in the position of the perpendicularly applied probe away from the receptive field focus led to a marked decline in responsiveness. 3. With appropriate choice of stimulus parameters for vibratory stimuli applied at the receptive field focus, the SAII fibres could respond at low threshold (< 100 microns), with a tightly phase‐locked, regular 1:1 impulse pattern (one impulse per vibration cycle) that accurately signalled the vibration frequency over a bandwidth that extended to 600 Hz. Furthermore, their responses remained phase‐locked up to 1000 Hz. Phase‐locking in SAII fibres was marginally tighter than that in SAI fibres and comparable to that of Pacinian corpuscle fibres. 4. The sensitivity of forelimb SAII fibres to tangential skin stretch was directionally selective; stretch across the forelimb was much more effective than along its long axis. Vibration associated with tangential skin stretch led to a marked spatial expansion of the field of vibration sensitivity. SAII fibres could therefore signal information about natural stimuli that contain elements of skin stretch and vibration, as may be encountered when the forelimb brushes against textured surfaces. Should the SAII fibres fail to contribute to the sensory experience of vibrotactile stimuli, the explanation may be related to limitations imposed centrally on the processing of their signals. Nevertheless, the present results demonstrate that, with appropriate stimulus conditions, the SAII afferent fibres have much greater vibrotactile sensitivity than has been suggested by past studies.

Corticocortical connections between area 21a and primary visual cortex in the cat

WE investigated the corticocortical connections between area 21a and ipsilateral areas 17 and 18 in the cat. The anterograde/retrograde fluorescent tracer tetramethylrhodamine conjugated to dextran (Fluoro-Ruby) was injected into area 21a of the anaesthetized cat. Cell bodies labelled retrogradely from area 21a were consistently observed in both areas 17 and 18, primarily located in the supragranular layers of cortex where they formed discrete patches of cells. Similar numbers of cell bodies were labelled retrogradely in areas 17 and 18 of each animal. Our data are also consistent with previous reports of a reciprocal projection from area 21a back to areas 17 and 18 terminating principally in infragranular cortical layers.

Binocular phase interactions in area 21a of the cat

1 Binocular interactions related to retinal disparity were investigated in single neurons in area 21a of extrastriate cortex in the anaesthetized cat using sinusoidal luminance gratings. 2 The responses of approximately two‐thirds of neurons were profoundly modulated by a relative phase difference between identical drifting gratings presented to each eye. This modulation included both facilitatory and inhibitory interocular interactions. The selectivity for binocular disparity was about twice as sharp as the selectivity for monocular spatial position. 3 Significant phase modulation was retained in many neurons at interocular orientation differences exceeding 45 deg. The response suppression associated with stimulation at a phase shift 180 deg from the optimum was stronger than the response suppression to an interocular orientation difference of 90 deg. 4 The proportion of phase modulated neurons and the potency of modulation in area 21a neurons exceed that reported for phase‐selective complex cells in area 17. Neurons in area 21a show sharp disparity tuning that is relatively insensitive to changes in orientation and monocular position, which suggests that this extrastriate region has a role in stereoscopic depth perception.