Stimulus-Rate Sensitivity Discerns Area 3b of the Human Primary Somatosensory Cortex

Previous studies have shown that the hemodynamic response of the primary somatosensory cortex (SI) to electrical median nerve stimulation doubles in strength when the stimulus rate (SR) increases from 1 to 5 Hz. Here we investigated whether such sensitivity to SR is homogenous within the functionally different subareas of the SI cortex, and whether SR sensitivity would help discern area 3b among the other SI subareas. We acquired 3-tesla functional magnetic resonance imaging (fMRI) data from nine healthy adults who received pneumotactile stimuli in 25-s blocks to three right-hand fingers, either at 1, 4, or 10 Hz. The main contrast (all stimulations pooled vs. baseline), applied to the whole brain, first limited the search to the whole SI cortex. The conjunction of SR-sensitive contrasts [4 Hz − 1 Hz] > 0 and [10 Hz − 1 Hz] > 0 ([4Hz − 1Hz] + [10Hz − 1Hz] > 0), applied to the SI cluster, then revealed an anterior-ventral subcluster that reacted more strongly to both 10-Hz and 4-Hz stimuli than to the 1-Hz stimuli. No other SR-sensitive clusters were found at the group-level in the whole-brain analysis. The site of the SR-sensitive SI subcluster corresponds to the canonical position of area 3b; such differentiation was also possible at the individual level in 5 out of 9 subjects. Thus the SR sensitivity of the BOLD response appears to discern area 3b among other subareas of the human SI cortex.     

Cortical Plasticity Induced by Spike-Triggered Microstimulation in Primate Somatosensory Cortex

Electrical stimulation of the nervous system for therapeutic purposes, such as deep brain stimulation in the treatment of Parkinson’s disease, has been used for decades. Recently, increased attention has focused on using microstimulation to restore functions as diverse as somatosensation and memory. However, how microstimulation changes the neural substrate is still not fully understood. Microstimulation may cause cortical changes that could either compete with or complement natural neural processes, and could result in neuroplastic changes rendering the region dysfunctional or even epileptic. As part of our efforts to produce neuroprosthetic devices and to further study the effects of microstimulation on the cortex, we stimulated and recorded from microelectrode arrays in the hand area of the primary somatosensory cortex (area 1) in two awake macaque monkeys. We applied a simple neuroprosthetic microstimulation protocol to a pair of electrodes in the area 1 array, using either random pulses or pulses time-locked to the recorded spiking activity of a reference neuron. This setup was replicated using a computer model of the thalamocortical system, which consisted of 1980 spiking neurons distributed among six cortical layers and two thalamic nuclei. Experimentally, we found that spike-triggered microstimulation induced cortical plasticity, as shown by increased unit-pair mutual information, while random microstimulation did not. In addition, there was an increased response to touch following spike-triggered microstimulation, along with decreased neural variability. The computer model successfully reproduced both qualitative and quantitative aspects of the experimental findings. The physiological findings of this study suggest that even simple microstimulation protocols can be used to increase somatosensory information flow.     

Responses of Primate Taste Cortex Neurons to the Astringent Tastant Tannic Acid

In order to advance knowledge of the neural control of feeding,we investigated the cortical representation of the taste oftannic acid, which produces the taste of astringency. It isa dietary component of biological importance particularly toarboreal primates. Recordings were made from 74 taste responsiveneurons in the orbitofrontal cortex. Single neurons were foundthat were tuned to respond to 0.001 M tannic acid, and representeda subpopulation of neurons that was distinct from neurons responsiveto the tastes of glucose (sweet), NaCl (salty), HCI (sour),quinine (bitter) and monosodium glutamate (umami). In addition,across the population of 74 neurons, tannic acid was as wellrepresented as the tastes of NaCI, HCI quinine or monosodiumglutamate. Multidimensional scaling analysis of the neuronalresponses to the tastants indicates that tannic acid lies outsidethe boundaries of the four conventional taste qualities (sweet,sour, bitter and salty). Taken together these data indicatethat the astringent taste of tannic acid should be consideredas a distinct taste quality, which receives a separate representationfrom sweet, salt, bitter and sour in the primate cortical tasteareas. Chem. Senses 21: 135–145, 1996.     

Responses in Primary Somatosensory Cortex of Rhesus Monkey to Controlled Application of Embossed Grating and Bar Patterns

Responses of 66 neurons in primary somatosensory cortex (SI) of three anesthetized monkeys (Macaca mulatto) were characterized with grating patterns of 550- to 2900-mm groove width (Gw) and 250-mm ridge width, and/or pairs of 3-mm-wide ridges (bars) spaced 1-20 mm apart. Surfaces were stroked across single fingertips at parametrically varied levels of force ('25-150 g) and velocity ('25-100 mm/sec). The average firing rates (AFRs) of many cells varied with Gw, but force and velocity altered response functions (e.g., from linear to plateau or inverted). Slowly adapting (SA) cells were more sensitive to force, rapidly adapting (RA) cells to velocity. Force and velocity affected all cells sensitive to Gw, which suggests that response independence (e.g., AFR correlated with Gw but not force or velocity) may require active touch

Discharge intervals of many cells replicated stimulus temporal period. This temporal fidelity in SAs far exceeded examples reported for active touch. However, discharge burst duration and AFR increased with Gw, supporting a neural rate rather than temporal code for roughness. Force and velocity altered the Gw at which some cells fired once in phase to stimulus cycle (“tuning point”). Responses to bar edges suggest cortical replication of peripheral mechanoreceptor sensitivity to skin curvature, leading to this temporal fidelity in some cortical cells. Graded RA responses to Gw without obvious stimulus temporal replication may reflect early stages of integrative processing in supra- and infragranular layers that blur obvious temporal patterning and lead to a rate code correlated with spatial variation and proportional to perceived roughness     

Temporal Sharpening of Sensory Responses by Layer V in the Mouse Primary Somatosensory Cortex

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Neuronal Responses in Ventroposterolateral Nucleus of Thalamus in Monkeys (Macaca mulatta) during Active Touch of Gratings

Responses of single neurons were recorded from the ventroposterolateral nucleus (VPL) of the thalamus while a monkey stroked its fingertips over gratings. Monkeys were trained to stroke the gratings with consistent downward applied force and velocity of hand motion. Neurons were selected with receptive fields on the glabrous digits. Average firing rate was computed for a range of grating groove widths; groove width corresponded to roughness. Force and velocity were measured. VPL responses were compared to previously reported responses in primary somatosensory cortex (SI) under identical stimulus conditions, and to reports of peripheral afferent fiber responses to passively applied gratings. VPL responses more closely resembled those of peripheral afferent fibers than those of SI in important respects: lack of independent responses to roughness, force, and velocity; high temporal and force fidelity; and response patterns that closely followed the shape of elevated metal strips used to separate pairs of gratings. The presence in cortex of response patterns not seen in the thalamus, such as response independence and negative correlations to groove width, suggests that they stem from cortical processing.     

The Effects of Localized Inactivation of Somatosensory Cortex,Area 2, on the Cat Motor Cortex

Direct corticocortical afferents to the primary motor cortex (MI) originate in area 2 and area 3a of the primary somatosensory cortex (SI). The functional and morphological characteristics of the two pathways indicate that they relay different sensory signals to MI. The role of area 2 in relaying peripheral information to the cat MI was studied using electrophysiological techniques. Neurons that responded to stimulation of peripheral receptive fields on the contralateral forepaw were identified in MI by extracellular recordings. In area 2 of SI, neurons with the same receptive field modality and location as those in MI were also identified. Field potentials to electrical stimulation of the peripheral receptive field were recorded at the somatotopically matched sites in both MI and SI. Neuronal activity at the recording site in area 2 was blocked by injection of lidocaine, a local anesthetic. Changes in MI and area 2 responses were monitored before and after inactivation of area 2. Neuronal activity near the injection site was abolished, and evoked potentials (EPs) in area 2 were considerably diminished immediately following the injection. In MI, spontaneous activity levels were altered at some sites, but overall these changes were not significant. MI EPs recorded in response to peripheral stimulation were altered, and various patterns of change were noted in the early and late phases of the EPs. Changes often occurred in only one phase of the response. In some EPs, both early and late phases changed, but the direction and magnitude of change in one phase were not always linked to such changes in the other phase. Both increases and decreases in the amplitude and the area of each phase were observed. The morphological characteristics of the projection were reviewed and related to the findings in the study. It is proposed that inherent features of the pathway may account for the variable patterns of change that were observed.     

Responses in the First or Second Somatosensory Cortical Area in Cats during Transient Inactivation of the Other Ipsilateral Area with Lidocaine Hydrochloride

Simultaneous recordings were obtained from the primary and secondary somatosensory cortical areas (SI and SII) in cats anesthetized with ketamine or pentobarbital. A total of 40 individual neurons were studied (29 in SII and 11 in SI) before, during, and following injections of microliter quantities of lidocaine hydrochloride in the other ipsilateral cortical area. Activity in the cortex injected with the local anesthetic was monitored with single-neuron, multi-neuron, or evoked potential responses to determine the time course of inactivation within 0.5-2 mm of the injection sites. Recording sites in both cortical locations were in the representations of the distal forelimb. Responses were elicited by transcutaneous electrical stimulation across the receptive fields with needle electrodes. Short-latency responses were synchronously activated, and, in those circumstances where single neurons were isolated in both areas, no overall differences in latency were noted. Anesthetization of either cortical area never blocked access of somatosensory information to the intact area, even when the injected cortex was completely silenced in the vicinity of the injection mass. In 15 SII neurons and 7 SI neurons, changes were seen in short-latency evoked responses to stimulation of their receptive fields or in background activity following local anesthesia of the other area through several cycles of injection and recovery. In 7 of these 15 SII cells, changes were noted in the timing and/or firing rates of the short-latency responses; changes were noted in the short-latency responses of 2 of these 7 SI cells while SII was silenced. In 11 SII and 6 SI cells, “background” activity that was recorded during the interstimulus intervals either increased (most cases) or decreased during local anesthesia of the other area. The results are discussed in reference to the hypothesis that primary sensory cortical areas feed information forward to secondary areas, and these feed back modulatory controls to the primary regions.     

Responses of Neurons of the Extrastriate Area 21b of the Cat Brain Cortex to Changes in Orientation of Moving Visual Stimuli

We studied the responses of neurons of the extrastriate cortical area 21b of the cat to changes in orientation of the movements of visual stimuli within the receptive field (RF) of the neuron under study. Our experiments demonstrated that 24 of 108 cells (22%) responded differentially to a certain extent to orientation of the movements of visual stimuli. As a whole, neurons of the area 21b did not demonstrate fine tuning on the optimum angle of orientation. In many cases, neuronal responses to different orientations of the movement of visual stimulus depended significantly on specific parameters of this stimulus (its shape, dimensions, and contrast). Some directionally sensitive neurons responded to a change in orientation of the movement of visual stimuli by modification of the index of directionality. We also studied spatial organization of the RF of neurons with the presentation of stationary visual stimuli. Comparison of the neuronal responses to a change in orientation of the movements of stimuli and to presentation of stationary stimuli showed that the correlation between the orientation sensitivity of the neuron under study and the stationary functional organization of its RF was insignificant. We hypothesize that inhibitory processes and subthreshold influences from a space surrounding the RF play a special role in the formation of the neuronal responses generated in the associative visual cortical regions to visual stimulation.     

The Arbors of Axons Terminating in Middle Cortical Layers of Somatosensory Area 3b in Owl Monkeys

The arbors of single axons terminating predominantly in layer IV of the representation of the hand in area 3b of owl monkeys were reconstructed from serial brain sections after axons beneath the cortex were severed and horseradish peroxidase was injected into the white matter. In addition to dense terminations in layer IV, these labeled axons generally had branches extending into deeper layer III, and a few had very sparse terminations in layer VI. Terminal arbors ranged from 100 to 900 μm in diameter, and fine branches with synaptic boutons were unevenly distributed, typically grouped in a large central cluster and one or more smaller side clusters. The results are consistent with three broad conclusions: (1) Since the arbors are large relative to the details of the somatotopic map in area 3b, all regions within a single arbor may not be equally effective in activating cortical cells. (2) Spatially separate branches of single axons may relate to spatially separate modules of neurons of the same class in a manner that allows them to receive the same inputs. (3) Many of the somatotopic changes that have been reported in the hand representation as a result of nerve manipulations in adults could result from alterations in synaptic effectiveness within the arbors of single axons.     

Shape Invariant Coding of Motion Direction in Somatosensory Cortex

Invariant representations of stimulus features are thought to play an important role in producing stable percepts of objects. In the present study, we assess the invariance of neural representations of tactile motion direction with respect to other stimulus properties. To this end, we record the responses evoked in individual neurons in somatosensory cortex of primates, including areas 3b, 1, and 2, by three types of motion stimuli, namely scanned bars and dot patterns, and random dot displays, presented to the fingertips of macaque monkeys. We identify a population of neurons in area 1 that is highly sensitive to the direction of stimulus motion and whose motion signals are invariant across stimulus types and conditions. The motion signals conveyed by individual neurons in area 1 can account for the ability of human observers to discriminate the direction of motion of these stimuli, as measured in paired psychophysical experiments. We conclude that area 1 contains a robust representation of motion and discuss similarities in the neural mechanisms of visual and tactile motion processing.     

Raphe Stimulation-Evoked Modulation of Postsynaptic Responses by Neurons of the Cat Somatosensory Cortex Activated by Stimulation of Nociceptors

We studied the effects of electrical stimulation of the raphe nuclei (RN) of the cat brain on postsynaptic potentials developing in somatosensory cortex neurons activated by nociceptive influences. Intracellular records were obtained from 15 cells, which were either selectively excited by stimulation of nociceptors (intense electrical stimulation of the dental pulp) or activated by both the above nociceptive and non-nociceptive (moderate stimulations of the infraorbital nerve or thalamic ventroposteromedial nucleus, VPMN) influences. In neurons of both groups, stimulation of both nociceptive afferents and the VPMN evoked complex responses (EPSP–AP–IPSP; IPSPs were 200 to 300 msec long). In some studied cortical neurons, isolated electrical stimulation of the RN (which caused the release of serotonin, 5-HT, in the cortex) resulted in relatively short-latency synaptic excitation, while inhibition was observed in other cells. In the case where stimulation of the RN was used as conditioning influence, such stimulation (independently of the kind of the initial response to RN stimulation) led to long-latency and long-lasting suppression of all components of the synaptic reactions evoked by excitation of nociceptors. The maximum of inhibition was observed at test intervals of 300 to 800 msec. The mechanisms underlying modulatory influences coming from the 5-HT-ergic brainstem system to neurons of the somatosensory cortex, which are activated by excitation of high-threshold (nociceptive) afferent inputs, are discussed.     

Axonal Dynamics of Excitatory and Inhibitory Neurons in Somatosensory Cortex

Cortical topography can be remapped as a consequence of sensory deprivation, suggesting that cortical circuits are continually modified by experience. To see the effect of altered sensory experience on specific components of cortical circuits, we imaged neurons, labeled with a genetically modified adeno-associated virus, in the intact mouse somatosensory cortex before and after whisker plucking. Following whisker plucking we observed massive and rapid reorganization of the axons of both excitatory and inhibitory neurons, accompanied by a transient increase in bouton density. For horizontally projecting axons of excitatory neurons there was a net increase in axonal projections from the non-deprived whisker barrel columns into the deprived barrel columns. The axon collaterals of inhibitory neurons located in the deprived whisker barrel columns retracted in the vicinity of their somata and sprouted long-range projections beyond their normal reach towards the non-deprived whisker barrel columns. These results suggest that alterations in the balance of excitation and inhibition in deprived and non-deprived barrel columns underlie the topographic remapping associated with sensory deprivation.     

Time Course of Functional Connectivity in Primate Dorsolateral Prefrontal and Posterior Parietal Cortex during Working Memory

The dorsolateral prefrontal and posterior parietal cortex play critical roles in mediating attention, working memory, and executive function. Despite proposed dynamic modulation of connectivity strength within each area according to task demands, scant empirical data exist about the time course of the strength of effective connectivity, particularly in tasks requiring information to be sustained in working memory. We investigated this question by performing time-resolved cross-correlation analysis for pairs of neurons recorded simultaneously at distances of 0.2–1.5 mm apart of each other while monkeys were engaged in working memory tasks. The strength of effective connectivity determined in this manner was higher throughout the trial in the posterior parietal cortex than the dorsolateral prefrontal cortex. Significantly higher levels of parietal effective connectivity were observed specifically during the delay period of the task. These differences could not be accounted for by differences in firing rate, or electrode distance in the samples recorded in the posterior parietal and prefrontal cortex. Differences were present when we restricted our analysis to only neurons with significant delay period activity and overlapping receptive fields. Our results indicate that dynamic changes in connectivity strength are present but area-specific intrinsic organization is the predominant factor that determines the strength of connections between neurons in each of the two areas.     

The Responses of Neurons of the Somatosensory Cortex to Stimulation of the Posterior Thalamus (PO) in WAG/Rij Rats Genetically Predisposed to Absence Epilepsy

In genetically predisposed WAG/Rij rats and healthy Wistar rats, we studied functioning of the paralemniscal region of the thalamo-cortical system. The responses of neurons of the somatosensory cortex to single electrical stimulation of the posterior nucleus of the thalamus were recorded in two- to three-monthold rats within the period when the epileptic activity was not developed. We revealed lower number of shortterm inhibitory responses in WAG/Rij rats as compared to Wistar rats. This may create preconditions for the spreading of spike-wave activity in the somatosensory cortex, which is an electrophysiological sign of absence epilepsy.