Coding of deflection velocity and amplitude by whisker primary afferent neurons: implications for higher level processing

Within the rat whisker-to-barrel pathway, local circuits in cortical layer IV are more sensitive to the initial timing of deflection-evoked thalamic responses than to the total number of spikes comprising them. Because thalamic response timing better reflects whisker deflection velocity than amplitude, cortical neurons are more responsive to the former than the latter. The aim of this study is to determine how deflection velocity and amplitude may be encoded by the primary afferent neurons innervating the vibrissae. Responses of 81 extracellularly recorded trigeminal ganglion neurons (60 slowly and 21 rapidly adapting) were studied using controlled whisker stimuli identical to those used previously to investigate the velocity and amplitude sensitivities of thalamic and cortical neurons. For either slowly (SA) or rapidly adapting (RA) neurons, velocity is reflected by both response magnitude, measured as the total number of evoked spikes/stimulus, and initial firing rate, measured as the number of spikes discharged during the first 2 ms of the response. Deflection amplitude, on the other hand, is represented only by the SA population in their response magnitudes. Thus, in both populations initial firing rates unambiguously reflect deflection velocity. Together with previous findings, results demonstrate that information about deflection velocity is preserved throughout the whisker-to-barrel pathway by central circuits sensitive to initial response timing.     

Physiology and morphology of descending neurons in pheromone-processing olfactory pathways in the male moth Manduca sexta

1. We have characterized the responses and structure of olfactory descending neurons (DNs) that reside in the protocerebrum (PC) of the brain of male sphinx moths Manduca sexta and project toward thoracic ganglia. 2. Excitatory responses of DNs to pheromone blends were of two general types: (a) brief excitation (BE) that recovered to background in less than 1 s after the stimulus, and (b) long-lasting excitation (LLE) that outlasted the stimulus by greater than or equal to 1 s and, in many cases, as long as 30 s. Individual pheromone components were ineffective in eliciting LLE. 3. Some neurons showing LLE also exhibited state-dependent responses to pheromonal stimuli. When such neurons were in a state of low background firing, stimulation with pheromone blend elicited LLE. When they were in a state of LLE, an identical stimulus reduced firing for 5-10 s after which firing gradually increased to the initial higher level. 4. Thirteen stained DNs were reconstructed from serial sections for detailed analysis of their morphology in the brain. DNs exhibiting LLE had neurites concentrated in the lateral accessory lobes (LALs) in the protocerebrum and adjacent neuropil. Most DNs exhibiting only BE to pheromonal stimuli and other DNs showing responses only to visual or mechanosensory stimuli did not have branches in the LALs.     

Cortical influences on neurons of the lateral reticular nucleus responding to noxious stimuli

The effect of frontoparietal sensorimotor (FPSM) cortex stimulation on both the spontaneous and the noxious evoked activity of neurons in the lateral reticular nucleus (LRN) was tested in barbiturate-anesthetized rats. Ninety-three LRN neurons that responded to a noxious heat stimulus (HS) were recorded (72% antidromically fired from the cerebellum). Of these, 66 neurons altered their spontaneous firing rates in response to cortical stimulation. Two patterns of responses were found: either an excitation followed by a suppression of spontaneous activity (52 neurons), or a pure suppression of spontaneous activity lasting 50-400 msec (14 neurons). In 46 of these neurons, it was found that cortical stimulation reduced HS-evoked activity to near the baseline level. Furthermore, it was found that when applied after a prolonged cortical stimulation, the HS was ineffective. It is concluded that FPSM cortex can influence nociceptive information in LRN neurons that respond to its stimulation, possibly interfering with the mechanisms underlying stimulation-produced analgesia (SPA). In this context, it is proposed that the cortex can modulate the activity of LRN neurons that activate, through local loops, a descending antinociceptive system and also a separate projection system to the cerebellum.     

Neural mechanisms of tactile motion integration in somatosensory cortex

How are local motion signals integrated to form a global motion percept? We investigate the neural mechanisms of tactile motion integration by presenting tactile gratings and plaids to the fingertips of monkeys, using the tactile analogue of a visual monitor and recording the responses evoked in somatosensory cortical neurons. The perceived directions of the gratings and plaids are measured in parallel psychophysical experiments. We identify a population of somatosensory neurons that exhibit integration properties comparable to those induced by analogous visual stimuli in area MT and find that these neural responses account for the perceived direction of the stimuli across all stimulus conditions tested. The preferred direction of the neurons and the perceived direction of the stimuli can be predicted from the weighted average of the directions of the individual stimulus features, highlighting that the somatosensory system implements a vector average mechanism to compute tactile motion direction that bears striking similarities to its visual counterpart.     

Tuned normalization explains the size of attention modulations

The effect of attention on firing rates varies considerably within a single cortical area. The firing rate of some neurons is greatly modulated by attention while others are hardly affected. The reason for this variability across neurons is unknown. We found that the variability in attention modulation across neurons in area MT of macaques can be well explained by variability in the strength of tuned normalization across neurons. The presence of tuned normalization also explains a striking asymmetry in attention effects within neurons: when two stimuli are in a neuron's receptive field, directing attention to the preferred stimulus modulates firing rates more than directing attention to the nonpreferred stimulus. These findings show that much of the neuron-to-neuron variability in modulation of responses by attention depends on variability in the way the neurons process multiple stimuli, rather than differences in the influence of top-down signals related to attention.     

Network interactions among sensory neurons in the leech

Interactions among mechanosensory neurons, sensitive to touch, pressure and nociceptive stimuli in the leech nervous system were studied in isolated ganglia and in body-wall preparations. Pairs of touch-pressure, touch-nociceptive and pressure-nociceptive neurons were tested by suprathreshold stimulation of one neuron while recording the response of the other, in both directions. Pressure and nociceptive stimulation evoked depolarizing and hyperpolarizing responses in touch cells, mediated by interneurons. The relative expression of these responses depended on the stimulus duration. One or two pressure cell spikes produced, predominantly, a depolarization of the touch cells, and increasing number of spikes evoked a hyperpolarization. Nociceptive cells produced primarily the hyperpolarization of touch cells at any stimulus duration. When touch cells were induced to fire by injection of positive current into the soma, stimulation of pressure cells inhibited touch cell activity. However, when touch cells were induced to fire by peripheral stimulation, pressure cell activation failed to inhibit touch cell firing. The results suggest that excitation of pressure and nociceptive cells would not limit the responses of touch cells to peripheral stimuli, but would inhibit the firing of touch cells evoked by their central connectivity network.     

A possible mechanism of participation of dopaminergic cells and striatal cholinergic interneurons in the conditioned selection of motor activity

A possible mechanism of participation of cholinergic striatal interneurons and dopaminergic cells in conditioned selection of a certain types of motor activity is proposed. This selection is triggered by simultaneous increase in the activity of dopaminergic cells and a pause in the activity of cholinergic interneurons in response to a conditioned stimulus. This pause is promoted by activation of striatal inhibitory interneurons and action of dopamine at D2 receptors on cholinergic cells. Opposite changes in dopamine and acetylcholine concentration synergistically modulate the efficacy of corticostriatal inputs, modulation rules for the "strong" and "weak" corticostriatal inputs are opposite. Subsequent reorganization of neuronal firing in the loop cortex--basal ganglia--thalamus--cortex results in amplification of activity of the group of cortical neurons that strongly activate striatal cells, and simultaneous suppression of activity of another group of cortical neurons that weakly activate striatal cells. These changes can underlie a conditioned selection of motor activity performed with involvement of the motor cortex. As follows from the proposed model, if the time delay between conditioned and unconditioned stimuli does not exceed the latency of responses of dopaminergic and cholinergic cells (about 100 ms), conditioned selection of motor activity and learning is problematic.     

Tactile-spatial and cross-modal attention effects in the second somatosensory and 7b cortical areas of rhesus monkeys

Abstract This study analyzed neuronal responses in the second somatosensory (SII) and 7b cortical areas during a selective attention task. Cues directed attention to one of three simultaneous stimuli: vibrotactile stimuli applied to mirror sites on both hands or to a similarly timed auditory tone. Two stimulus patterns appeared with equal probability for the cued stimulus: a constant amplitude sinewave or the latter with a superimposed brief amplitude pulse midway in the trial. Uncued stimuli always contained amplitude pulses. Monkeys demonstrated whether an amplitude pulse at the cued location was present or absent by making appropriately rewarded up and down foot pedal movements. Cue location and stimulus pattern varied trial-wise and pseudo-randomly. Average firing rates to vibrotactile stimuli in 82 of 181 SII cells and 13 of 22 area 7b cells differed significantly during at least one epoch for trials cued to the contralateral hand when compared to trials cued to the ipsilateral hand or auditory stimulus. Predominant were relatively suppressed firing rates during times prior to the epoch containing the amplitude pulses or enhanced activity during and after these pulses. Generally, different cells showed suppression early vs enhancement later in a trial. Analyses of the ratio between firing rates before and during the amplitude pulses suggested improved evoked signals to the amplitude pulses. The discussion considers attention as a mechanism for reducing distractions, early in the trial through suppressing these signals, or for selectively increasing response magnitudes in the cued channel, especially around times when amplitude pulses were present or absent.     

Whisker plucking alters responses of rat trigeminal ganglion neurons

Whisker plucking in developing and adult rats provides a convenient method of temporarily altering tactile input for the purposes of studying experience-dependent plasticity in the somatosensory cortex. Yet, a comprehensive examination of the effect of whisker plucking on the response properties of whisker follicle-innervating trigeminal ganglion (NVg) neurons is lacking. We used extracellular single unit recordings to examine responses of NVg neurons to controlled whisker stimuli in three groups of animals: (1) rats whose whiskers were plucked from birth for 21 days; (2) rats whose whiskers were plucked once at 21 days of age; and (3) control animals. After at least 3 weeks of whisker re-growth, NVg neurons in plucked rats displayed normal, single whisker receptive fields and could be characterized as slowly (SA) or rapidly adapting (RA). The proportion of SA and RA neurons was unaffected by whisker plucking. Both SA and RA NVg neurons in plucked rats displayed normal response latencies and angular tuning but abnormally large responses to whisker movement onsets and offsets. SA neurons were affected to a greater extent than RA neurons. The effect of whisker plucking was more pronounced in animals whose whiskers were plucked repeatedly during development than in rats whose whiskers were plucked once. Individual neurons in plucked animals displayed abnormal periods of prolonged rhythmic firing following deflection onsets and aberrant bursts of activity during the plateau phase of the stimulus. These results indicate that whisker plucking exerts a long-term effect on responses of trigeminal ganglion neurons to peripheral stimulation.     

Whisker plucking alters responses of rat trigeminal ganglion neurons

Whisker plucking in developing and adult rats provides a convenient method of temporarily altering tactile input for the purposes of studying experience-dependent plasticity in the somatosensory cortex. Yet, a comprehensive examination of the effect of whisker plucking on the response properties of whisker follicle-innervating trigeminal ganglion (NVg) neurons is lacking. We used extracellular single unit recordings to examine responses of NVg neurons to controlled whisker stimuli in three groups of animals: (1) rats whose whiskers were plucked from birth for 21 days; (2) rats whose whiskers were plucked once at 21 days of age; and (3) control animals. After at least 3 weeks of whisker re-growth, NVg neurons in plucked rats displayed normal, single whisker receptive fields and could be characterized as slowly (SA) or rapidly adapting (RA). The proportion of SA and RA neurons was unaffected by whisker plucking. Both SA and RA NVg neurons in plucked rats displayed normal response latencies and angular tuning but abnormally large responses to whisker movement onsets and offsets. SA neurons were affected to a greater extent than RA neurons. The effect of whisker plucking was more pronounced in animals whose whiskers were plucked repeatedly during development than in rats whose whiskers were plucked once. Individual neurons in plucked animals displayed abnormal periods of prolonged rhythmic firing following deflection onsets and aberrant bursts of activity during the plateau phase of the stimulus. These results indicate that whisker plucking exerts a long-term effect on responses of trigeminal ganglion neurons to peripheral stimulation.     

Tactile-spatial and cross-modal attention effects in the primary somatosensory cortical areas 3b and 1-2 of rhesus monkeys

Neuronal responses in somatosensory cortical areas 3b and 1-2 (S1) were recorded during an attention task involving cue directed selection of one of three simultaneous stimuli: dual sinewave shaped vibrotactile stimuli applied to mirror sites on both hands or a similarly timed auditory tone. The cued stimulus occurred with one of two equally probable patterns: a constant amplitude vibration or the latter with a superimposed brief sinewave amplitude pulse midway during stimulation. Uncued stimuli always contained amplitude pulses. Two monkeys signaled the absence or presence of an amplitude pulse by appropriately moving a foot pedal up or down. Cues initiated trials by marking the location where the monkey had to discriminate the stimulus pattern. Cue location and stimulus pattern varied randomly per trial. Approximately 50% of cells (44/77 in 3b and 39/77 in 1-2) had significantly different firing rates to stimulation cued to the contralateral hand relative to spatially cuing the ipsilateral hand or cross-modally the auditory stimulus. Relatively suppressed firing rates during times prior to the epoch containing amplitude pulses improved signal-to-noise ratios for responses to amplitude pulses. Instances of significant enhanced activity during and after intervals with amplitude pulses were rare and relative to suppressed activity when cues directed attention to the ipsilateral hand or auditory stimulus. The present findings suggest that attention influences even the earliest stage somatosensory cortical processing. Findings were more modest in S1 than those previously seen in S2 (Burton et al., Somatosens Mot Res 14: 237-267, 1997), which supports the concept of multistage attention processes for touch.     

Persistence of Cortical Sensory Processing during Absence Seizures in Human and an Animal Model: Evidence from EEG and Intracellular Recordings

Absence seizures are caused by brief periods of abnormal synchronized oscillations in the thalamocortical loops, resulting in widespread spike-and-wave discharges (SWDs) in the electroencephalogram (EEG). SWDs are concomitant with a complete or partial impairment of consciousness, notably expressed by an interruption of ongoing behaviour together with a lack of conscious perception of external stimuli. It is largely considered that the paroxysmal synchronizations during the epileptic episode transiently render the thalamocortical system incapable of transmitting primary sensory information to the cortex. Here, we examined in young patients and in the Genetic Absence Epilepsy Rats from Strasbourg (GAERS), a well-established genetic model of absence epilepsy, how sensory inputs are processed in the related cortical areas during SWDs. In epileptic patients, visual event-related potentials (ERPs) were still present in the occipital EEG when the stimuli were delivered during seizures, with a significant increase in amplitude compared to interictal periods and a decrease in latency compared to that measured from non-epileptic subjects. Using simultaneous in vivo EEG and intracellular recordings from the primary somatosensory cortex of GAERS and non-epileptic rats, we found that ERPs and firing responses of related pyramidal neurons to whisker deflection were not significantly modified during SWDs. However, the intracellular subthreshold synaptic responses in somatosensory cortical neurons during seizures had larger amplitude compared to quiescent situations. These convergent findings from human patients and a rodent genetic model show the persistence of cortical responses to sensory stimulations during SWDs, indicating that the brain can still process external stimuli during absence seizures. They also demonstrate that the disruption of conscious perception during absences is not due to an obliteration of information transfer in the thalamocortical system. The possible mechanisms rendering the cortical operation ineffective for conscious perception are discussed, but their definite elucidation will require further investigations.     

Encoding Stimulus Information by Spike Numbers and Mean Response Time in Primary Auditory Cortex

Neurons can transmit information about sensory stimuli via their firing rate, spike latency, or by the occurrence of complex spike patterns. Identifying which aspects of the neural responses actually encode sensory information remains a fundamental question in neuroscience. Here we compared various approaches for estimating the information transmitted by neurons in auditory cortex in two very different experimental paradigms, one measuring spatial tuning and the other responses to complex natural stimuli. We demonstrate that, in both cases, spike counts and mean response times jointly carry essentially all the available information about the stimuli. Thus, in auditory cortex, whereas spike counts carry only partial information about stimulus identity or location, the additional availability of relatively coarse temporal information is sufficient in order to extract essentially all the sensory information available in the spike discharge pattern, at least for the relatively short stimuli (< ∼ 100 ms) commonly used in auditory research.     

Associative fear learning enhances sparse network coding in primary sensory cortex

Several models of associative learning predict that stimulus processing changes during association formation. How associative learning reconfigures neural circuits in primary sensory cortex to "learn" associative attributes of a stimulus remains unknown. Using 2-photon in vivo calcium imaging to measure responses of networks of neurons in primary somatosensory cortex, we discovered that associative fear learning, in which whisker stimulation is paired with foot shock, enhances sparse population coding and robustness of the conditional stimulus, yet decreases total network activity. Fewer cortical neurons responded to stimulation of the trained whisker than in controls, yet their response strength was enhanced. These responses were not observed in mice exposed to a nonassociative learning procedure. Our results define how the cortical representation of a sensory stimulus is shaped by associative fear learning. These changes are proposed to enhance efficient sensory processing after associative learning.     

Areal and callosal connections in the somatosensory cortex of the star-nosed mole

Star-nosed moles have a well-developed somatosensory cortex with multiple cortical areas representing the behaviorally important tactile star. In each of three cortical representations, the 11 mechanosensory appendages from the contralateral nose are represented in a series of dark cytochrome oxidase modules. Here the connections of this complex cortical network were explored with injections of the neuroanatomical tracer wheat germ agglutinin conjugated to horseradish peroxidase (WGA-H RP). The main goal was to determine the connection patterns of the somatosensory areas that represent the star. Injections of tracer made in or around the primary somatosensory representation (S1) of the star allowed us to determine the topography of local cortical connections and the projection and termination sites of corresponding interhemispheric connections. The results revealed precise topographic corticocortical connections reciprocally interconnecting the S1 star representation with its counterparts in S2 and in a third representation (S3) unique to star-nosed moles. Callosal connections from a widespread area of the contralateral hemisphere terminated primarily in the septa between cytochrome oxidase dark modules and in areas of cortex surrounding the star representations. However, midline structures of the star represented in S1 and S2 exhibited a high level of callosally labeled cells and terminals. This included label both within septa and within the centers of cytochrome oxidase dense modules representing midline appendages.     

Responses of parietal associative neurons to stimulation of primary sensory areas

Responses of 251 neurons in the anterior part of the middle suprasylvian gyrus to stimulation of primary sensory (auditory, visual, somatosensory) areas and also to acoustic, visual, and somatosensory stimuli were studied in acute experiments on cats anesthetized with chloralose (40 mg/kg) and pentobarbital (20 mg/kg). Three groups of neurons were distinguished by their responses to stimulation of the primary sensory areas: those responding by an increased firing rate (117) or by inhibition (35) and those not responding (99). Responses of 193 neurons to stimulation of the peripheral afferent systems were analyzed. Neurons of the parietal associative cortex responded more frequently to cortical stimulation than to peripheral. By the duration of the latent period of their response to cortical stimulation the neurons were divided into three groups: those with short (less than 20 msec), medium (20–30 msec), and long latent periods (over 30 msec). The first group was the largest.Kemerovo State Medical Institute. Translated from Neirofiziologiya, Vol. 4, No. 5, pp. 524–530, September–October, 1972.     

Exploring the cortical evidence of a sensory-discrimination process

Humans and monkeys have similar abilities to discriminate the difference in frequency between two consecutive mechanical vibrations applied to their fingertips. This task can be conceived as a chain of neural operations: encoding the two consecutive stimuli, maintaining the first stimulus in working memory, comparing the second stimulus with the memory trace left by the first stimulus and communicating the result of the comparison to the motor apparatus. We studied this chain of neural operations by recording and manipulating neurons from different areas of the cerebral cortex while monkeys performed the task. The results indicate that neurons of the primary somatosensory cortex (S1) generate a neural representation of vibrotactile stimuli which correlates closely with psychophysical performance. Discrimination based on microstimulation patterns injected into clusters of S1 neurons is indistinguishable from that produced by natural stimuli. Neurons from the secondary somatosensory cortex (S2), prefrontal cortex and medial premotor cortex (MPC) display at different times the trace of the first stimulus during the working-memory component of the task. Neurons from S2 and MPC appear to show the comparison between the two stimuli and correlate with the behavioural decisions. These neural operations may contribute to the sensory-discrimination process studied here.     

Meeting report

Neuronal responses in somatosensory cortical areas 3b and 1- 2 (S1) were recorded during an attention task involving cue directed selection of one of three simultaneous stimuli: dual sinewave shaped vibrotactile stimuli applied to mirror sites on both hands or a similarly timed auditory tone. The cued stimulus occurred with one of two equally probable patterns: a constant amplitude vibration or the latter with a superimposed brief sinewave amplitude pulse midway during stimulation. Uncued stimuli always contained amplitude pulses. Two monkeys signaled the absence or presence of an amplitude pulse by appropriately moving a foot pedal up or down. Cues initiated trials by marking the location where the monkey had to discriminate the stimulus pattern. Cue location and stimulus pattern varied randomly per trial. Approximately 50% of cells (44/77 in 3b and 39/77 in 1- 2) had significantly different firing rates to stimulation cued to the contralateral hand relative to spatially cuing the ipsilateral hand or cross-modally the auditory stimulus. Relatively suppressed firing rates during times prior to the epoch containing amplitude pulses improved signal-to-noise ratios for responses to amplitude pulses. Instances of significant enhanced activity during and after intervals with amplitude pulses were rare and relative to suppressed activity when cues directed attention to the ipsilateral hand or auditory stimulus. The present findings suggest that attention influences even the earliest stage somatosensory cortical processing. Findings were more modest in S1 than those previously seen in S2 (Burton et al. , Somatosens Mot Res 14 : 237-267, 1997), which supports the concept of multistage attention processes for touch.     

Evidence for Synchronous Activation of Neurons Located in Different Layers of Primary Somatosensory Cortex

Although many studies have examined the columnar organization of primary somatosensory (SI) cortex, the functional relationship among neurons in different layers remains unclear. To understand how activity is coordinated among different cortical layers, the present investigation tested the hypothesis that the initial part of a peripheral stimulus produces a serial pattern of laminar activation in SI cortex. Extracellular discharges of 334 histologically recovered neurons were recorded from the medial bank of the coronal sulcus in nine anesthetized cats during electrical or cutaneous stimulation of the distal forelimb. Mean responses during the initial 50-msec period following stimulus onset were largest in layers IIIb or IV for both types of stimulation, but laminar differences in the magnitude of onset responses were not statistically significant. Among 175 neurons with responses exceeding 0.5 spikes per stimulus, electrical Stimulation consistently produced shorter response latencies than mechanical indentation in the extragranular (II, IIIa, V, VI), but not in the middle (IIIb, IV), cortical layers. The average minimum latencies for different cortical layers ranged from 7.4 to 10.1 msec for responses to electrical stimulation and from 10.3 to 11.6 msec for responses to mechanical indentations, but these laminar differences were not statistically significant. In some experiments, neurons in different layers of a cortical column were recorded simultaneously with dual-electrode assemblies; among 37 neuron pairs in which both neurons responded with more than 0.5 spikes per stimulus, response latencies were similar, even though the neurons were separated by several hundred microns. Cross-correlation analysis of the onset responses for neurons recorded simultaneously from different layers also indicated that many cells throughout a cortical column were activated nearly simultaneously by the initial phase of a peripheral stimulus. Results from the present study are compared with previous reports examining laminar patterns of activation.     

Medullary electrosensory processing in the little skate

1. Ampullary electroreceptors in elasmobranchs are innervated by fibers of the ALLN, which projects to the dorsal octavolateralis nucleus (DON). The purpose of this study is to examine the response characteristics of ALLN fibers and DON neurons to weak D.C. and sinusoidal electric field stimuli presented as local dipole fields. 2. ALLN fibers respond to presentation of D.C. fields with a phasic burst, followed by a more slowly adapting period of firing. Ascending efferent neurons (AENs) in the DON respond to stimuli with a similar initial burst, which adapts more quickly. 3. Type 1, 2, and 3 neurons are possible local interneurons or commissural DON neurons. Type 1 neurons demonstrate response properties similar to those of AENs. Type 2 cells demonstrated slowly adapting responses to excitatory stimuli, the duration of the response increased with the amplitude of the stimulus. Type 3 neurons demonstrated an increased rate of firing, but the response lacked any specific temporal characteristics. 4. ALLN fibers typically have receptive fields consisting of a single ampulla. The receptive field sizes of DON neurons exhibited varying degrees of convergence for different cell types. 5. Responses of ALLN fibers and DON neurons to weak sinusoidal stimuli demonstrated very similar frequency response characteristics for all cell types. The peak sensitivity of electrosensory neurons was between 5-10 Hz.