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.     

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.     

Effects on discrimination performance of selective attention to tactile features

This study examined selective attention to tactile dimensions by combining a selective cueing paradigm with a test of integrality. In Experiment 1, subjects selectively attended to changes in the frequency or duration of pairs of vibrotactile stimuli and identified the higher frequency or longer duration stimulus. In Experiment 2, using surface gratings in an identical experimental procedure, subjects identified the rougher or longer duration stimulus. In both experiments, greater performance accuracy was found on trials where the cue correctly (valid) predicted the changing dimension, vs incorrectly (invalid) cued or no-cue (neutral) trials. More errors on the invalidly vs neutrally cued trials show the cost of focal attention. Increases in performance on validly vs neutrally cued trials show a benefit of filtering irrelevant stimuli in the cued conditions. Results effectively demonstrate focal attention to tactile features. Tests of integrality, in terms of the effects of correlated change in both dimensions, showed no redundancy gain for either vibrotactile or grating tasks, suggesting that frequency and roughness are separable from stimulus duration. Interference of negative correlated change for frequency but not roughness discriminations may be explained by differences in task difficulty.     

Effects on discrimination performance of selective attention to tactile features

This study examined selective attention to tactile dimensions by combining a selective cueing paradigm with a test of integrality. In Experiment 1, subjects selectively attended to changes in the frequency or duration of pairs of vibrotactile stimuli and identified the higher frequency or longer duration stimulus. In Experiment 2, using surface gratings in an identical experimental procedure, subjects identified the rougher or longer duration stimulus. In both experiments, greater performance accuracy was found on trials where the cue correctly (valid) predicted the changing dimension, vs incorrectly (invalid) cued or no-cue (neutral) trials. More errors on the invalidly vs neutrally cued trials show the cost of focal attention. Increases in performance on validly vs neutrally cued trials show a benefit of filtering irrelevant stimuli in the cued conditions. Results effectively demonstrate focal attention to tactile features. Tests of integrality, in terms of the effects of correlated change in both dimensions, showed no redundancy gain for either vibrotactile or grating tasks, suggesting that frequency and roughness are separable from stimulus duration. Interference of negative correlated change for frequency but not roughness discriminations may be explained by differences in task difficulty.     

The effects of cross-modal manipulations of attention on the detection of vibrotactile stimuli in humans

Although it is well known that attention to a visual or auditory stimulus can enhance its perception, less is known concerning the effects of attention on the perception of natural tactile stimuli. The present study was conducted to examine the magnitude of the effect of cross-modal manipulations of attention in human subjects on the detection of weak, low-frequency vibrotactile stimuli delivered to the glabrous skin of the finger pad of the right index finger via an Optacon. Three suprathreshold vibrotactile arrays (40 Hz), varying in the number of activated pegs and hence the area of skin stimulated, were used. Subjects were trained to detect the occurrence of vibrotactile or visual stimuli and to respond by pressing a foot pedal as quickly as possible thereafter. Two instructional lights were used to cue the subjects as to which stimulus modality they should attend, in three experimental conditions. In the first cue condition, the forthcoming stimulus modality was indicated by the illumination of its associated light. In the second cue condition, both instructional lights were illuminated, and the subjects were asked to divide their attention equally between the two modalities. In the third cue condition, the stimulus modality was falsely indicated by the illumination of the cue not associated with the stimulus to be presented. Reaction times (RTs) were calculated for each trial. For each modality, tactile and visual, the RTs varied significantly with the cue condition, with the mean RT changing in a graded manner across the experimental conditions (being shortest for the correctly cued condition, intermediate for the neutrally cued condition, and longest for the incorrectly cued condition.(ABSTRACT TRUNCATED AT 250 WORDS)     

Phantoms in the brain: Ambiguous representations of stimulus amplitude and timing in weakly electric fish

In wave-type weakly electric fish, two distinct types of primary afferent fibers are specialized for separately encoding modulations in the amplitude and phase (timing) of electrosensory stimuli. Time-coding afferents phase lock to periodic stimuli and respond to changes in stimulus phase with shifts in spike timing. Amplitude-coding afferents fire sporadically to periodic stimuli. Their probability of firing in a given cycle, and therefore their firing rate, is proportional to stimulus amplitude. However, the spike times of time-coding afferents are also affected by changes in amplitude; similarly, the firing rates of amplitude-coding afferents are also affected by changes in phase. Because identical changes in the activity of an individual primary afferent can be caused by modulations in either the amplitude or phase of stimuli, there is ambiguity regarding the information content of primary afferent responses that can result in ‘phantom’ modulations not present in an actual stimulus. Central electrosensory neurons in the hindbrain and midbrain respond to these phantom modulations. Phantom modulations can also elicit behavioral responses, indicating that ambiguity in the encoding of amplitude and timing information ultimately distorts electrosensory perception. A lack of independence in the encoding of multiple stimulus attributes can therefore result in perceptual illusions. Similar effects may occur in other sensory systems as well. In particular, the vertebrate auditory system is thought to be phylogenetically related to the electrosensory system and it encodes information about amplitude and timing in similar ways. It has been well established that pitch perception and loudness perception are both affected by the frequency and intensity of sounds, raising the intriguing possibility that auditory perception may also be affected by ambiguity in the encoding of sound amplitude and timing.     

Manifestations of dynamic coding of the amplitude-modulated sounds on the level of auditory nerve fibres

Average firing rate of the auditory nerve fiber as function of the level of the tone with the frequency equal to characteristic frequency of the fibers, can be defined as an input-output characteristic. It is known that the steepening of the input-output characteristic of the real auditory nerve fiber is more, and the width is less than the spontaneous activity of the fiber. The latter characterizes fiber's ability to generate spikes, if the stimulus is absent. However it is known, that the real auditory nerve fibers with low spontaneous activity reproduce amplitude modulation of the signals much better, than the fibers with high spontaneous activity. From the results of simulation experiments, it follows that the dynamic properties of the auditory nerve fibers, providing fine tuning or adaptation of a fiber threshold under the stimulus level but not the static input-output characteristics, are the reason of fibers reproduction of stimuli amplitude modulations. However the auditory nerve fibers with high spontaneous activity due to abrupt input-output characteristic are capable to reproduce modulations of sounds whose levels are lower than a threshold of the fiber, if a weak signal adds to a weak broadband noise. This is a phenomenon of stochastic resonance found in the reactions of auditory nerve fibers.     

Encoding and decoding amplitude-modulated cochlear implant stimuli—a point process analysis

Cochlear implant speech processors stimulate the auditory nerve by delivering amplitude-modulated electrical pulse trains to intracochlear electrodes. Studying how auditory nerve cells encode modulation information is of fundamental importance, therefore, to understanding cochlear implant function and improving speech perception in cochlear implant users. In this paper, we analyze simulated responses of the auditory nerve to amplitude-modulated cochlear implant stimuli using a point process model. First, we quantify the information encoded in the spike trains by testing an ideal observer’s ability to detect amplitude modulation in a two-alternative forced-choice task. We vary the amount of information available to the observer to probe how spike timing and averaged firing rate encode modulation. Second, we construct a neural decoding method that predicts several qualitative trends observed in psychophysical tests of amplitude modulation detection in cochlear implant listeners. We find that modulation information is primarily available in the sequence of spike times. The performance of an ideal observer, however, is inconsistent with observed trends in psychophysical data. Using a neural decoding method that jitters spike times to degrade its temporal resolution and then computes a common measure of phase locking from spike trains of a heterogeneous population of model nerve cells, we predict the correct qualitative dependence of modulation detection thresholds on modulation frequency and stimulus level. The decoder does not predict the observed loss of modulation sensitivity at high carrier pulse rates, but this framework can be applied to future models that better represent auditory nerve responses to high carrier pulse rate stimuli. The supplemental material of this article contains the article’s data in an active, re-usable format.     

Responses of neurons in somatosensory cortical area II of cats to high-frequency vibratory stimuli during iontophoresis of a GABA antagonist and glutamate

Areas in the second somatic sensory cortex (SII) of cats that responded vigorously to low-amplitude, high-frequency vibratory stimulation were mapped with respect to the surrounding somatotopic organization. Neurons with these properties were found in the posterior and medial parts of the distal forelimb zone and were judged as receiving input from Pacinian mechanoreceptors. The responses of these neurons to sinusoidal vibrotactile stimulation were studied during iontophoretic administration of glutamate or bicuculline methiodide (BMI) to determine if the temporal fidelity of these cortical neurons was controlled by inhibitory circuits that used gamma-aminobutyric acid (GABA) as a neurotransmitter. The data from 19 Pacinian-sensitive neurons were analyzed for changes in the mean firing rate, the percentage of entrainment, and the pattern of periodicity as revealed by autocorrelograms and interval histograms. Iontophoresis of BMI or glutamate caused significant increases in mean firing rates during low- and high-frequency vibratory stimulation. The pattern of increased activity produced by BMI was characterized by a small, yet significant, reduction in the percentage of entrainment, whereas glutamate caused smaller and fewer significant changes in this measure. Analysis of autocorrelation and interval histograms suggested that BMI increased the probability of firing on consecutive stimulus cycles in small segments of the stimulus duration.     

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.     

Evoked potentials in the brain of adolescents in norm and those with attention deficit during recognition of short-term acoustic stimuli

The effect of stimulus duration on auditory event-related potentials and performance of oddball task was studied in normal children and those with attention-deficit symptoms. Mismatch negativity was absent on presentation of short-term (11 ms) stimuli and present with longer stimuli (50 ms). The adolescents with deficit of attention performed much worse (errors of omission) with the short stimuli. The RT was significantly larger in subjects with attention-deficit with all types of tested stimulus duration. They also manifested a smaller P3b amplitude in response to task-relevant deviant stimuli and larger N2b peaks in response to the standard stimuli. It was possible to differentiate between the MMN and the N2b components owing to the fact that the MMN was absent with shorter stimuli. The findings suggest that there is a deficit in processing of sensory information at the cortical level in subjects with the attention-deficit symptoms.     

A ratio code for vibrotactile pitch

Subjective impressions of pitch for 80 different sinusoidal vibrotactile stimuli delivered to the index finger were measured by free magnitude estimation in four subjects. In three of the subjects, pitch at a given frequency decreased as stimulus amplitude increased. The data of these subjects were well described by a model of pitch based on the relative levels of activation of the three major tactile channels. The main element in this model was a ratio of P channel activity to the sum of the activity levels of the P, NPI, and NPIII channels. Activity levels of the channels were estimated on the basis of the psychophysical literature, including a study of vibrotactile loudness using the same subjects and stimuli as those employed here. A fourth subject, whose pattern of loudness judgments had previously been shown to differ from those of the other subjects, did not conform to this pitch model: her data revealed significant increases in pitch with increases in amplitude, and appear to reflect an inability to combine signals across vibrotactile channels. Pitch changes resulting from vibrotactile adaptation were directionally consistent with our ratio model: pitch was slightly increased by adaptation to a 25 Hz stimulus, and slightly decreased by 200 Hz adaptation.     

Effects of attention and slow potential shifts on self-regulation of event-related potentials

Research on the effects of self-regulation of slow potentials (SP) and event-related potentials (ERP) has failed to look at the possible interactions of these two kinds of brain potentials. The present study investigated such interactions by recording both ERP and SP potential changes in an operant ERP conditioning paradigm. Ten subjects participated in two conditions that were designed to differentially manipulate attention to the stimuli. In the operant conditioning task, subjects received auditory feedback as they attempted to increase the ERP amplitude at 180 msec poststimulus (P180), which was elicited by a subpainful shock stimulus to the forearm over 250 trials. In the distraction task, subjects were instructed not to attend to stimuli or feedback tones, but rather received and were tested on reading materials. Attention, as manipulated by these tasks, was not a determinant of changes in ERP amplitude since there were no significant differences in the size of P180 between attention conditions. While no significant change in the mean ERP amplitude occurred, subjects were able to produce ERPs above criterion threshold significantly more often during trials in the conditioning task than in the reading task. Thus, there was evidence of some learning. The difference in wave forms between hit and miss trials indicates a latency shift (with misses having a later ERP peak). This may indicate that latency, rather than, or in addition to, amplitude, is shaped during conditioning procedures. In addition, the CNV that developed between the shock stimulus and the feedback signal during conditioning was significantly larger in amplitude than in the distraction condition. This is taken as evidence of increased attention during conditioning. Since hit trials demonstrated larger contingent negative variation (CNV) amplitudes, production of CNVs may be instrumental in mediating hits. Therefore, attentional mechanisms may play a role in successful ERP self-regulation. No correlations were found involving P180, CNVs, or tonic slow potential shifts. Changes in tonic DC levels showed a suggestive trend between conditions. Although both conditions began with a negative shift, during conditioning the negativity increased, while during distraction the tonic level went to positivity. These trends support the hypothesis that attention and arousal increased during conditioning. The possible reasons for the lack of significant correlations between ERP and tonic or phasic slow potential changes in this paradigm are discussed.     

A New Approach for Determining Phase Response Curves Reveals that Purkinje Cells Can Act as Perfect Integrators

Cerebellar Purkinje cells display complex intrinsic dynamics. They fire spontaneously, exhibit bistability, and via mutual network interactions are involved in the generation of high frequency oscillations and travelling waves of activity. To probe the dynamical properties of Purkinje cells we measured their phase response curves (PRCs). PRCs quantify the change in spike phase caused by a stimulus as a function of its temporal position within the interspike interval, and are widely used to predict neuronal responses to more complex stimulus patterns. Significant variability in the interspike interval during spontaneous firing can lead to PRCs with a low signal-to-noise ratio, requiring averaging over thousands of trials. We show using electrophysiological experiments and simulations that the PRC calculated in the traditional way by sampling the interspike interval with brief current pulses is biased. We introduce a corrected approach for calculating PRCs which eliminates this bias. Using our new approach, we show that Purkinje cell PRCs change qualitatively depending on the firing frequency of the cell. At high firing rates, Purkinje cells exhibit single-peaked, or monophasic PRCs. Surprisingly, at low firing rates, Purkinje cell PRCs are largely independent of phase, resembling PRCs of ideal non-leaky integrate-and-fire neurons. These results indicate that Purkinje cells can act as perfect integrators at low firing rates, and that the integration mode of Purkinje cells depends on their firing rate.     

Response of cortical evoked potentials to electric stimulation of the acoustic nerve in animals with damaged cochlea

Evoked potentials of the auditory cortex during the electrical stimulation of the cochlea were studied in acute experiments on cats. A series of electric pulses of short duration and different frequency delivered to the streptomycin-damaged cochlea were used as a stimulus. It has been shown that an amplitude and latency of electrical cortex responses depended on the number of pulses in series and on the interpulse intervals. Amplitudes of evoked responses increased with the growth of the number of stimuli. Latent periods changed in a narrower stimulation frequency band. Dependence of the induced potentials' amplitude growth on the increase in the number of electric pulses changed as a result of the two-fold enhancement of the stimulation amplitude.     

Auditory steady-state responses to multiple simultaneous stimuli

Steady-state responses can follow multiple simultaneous auditory stimuli. If the stimuli are modulated at different rates, responses specific to each stimulus can be assessed by measuring in the frequency domain response the spectral component corresponding to the rate of modulation. When each stimulus has a different carrier frequency or different ear of presentation, the responses when 8 stimuli are presented simultaneously are not significantly different than when each stimulus is presented alone. Since significant responses can be recognized down to intensities that average 14 dB above behavioral threshold, this technique may be useful in objective audiometry. It is also possible to record steady-state responses to multiple modulations of the same carrier frequency. In this case, the amplitude of the responses when the stimuli are combined is smaller than when the stimuli are presented alone. The decrease in amplitude depends upon the number of concomitant stimuli and their relative intensities. These effects are probably due to the compressive rectification occurring during cochlear transduction, and the data may be used to model cochlear processing of auditory stimuli.     

Chemical and thermal stimuli have short-lived effects on the retzius cell in the medicinal leech

During the appetitive phase of feeding, hungry leeches detect a prey by the integration of signals perceived by different sensory systems. Earlier reports suggested that chemical or thermal sensory stimulation of the lip was associated with increased afferent activity in cephalic nerves connecting the lip to the central nervous system. These authors further suggested that this activity was relayed to Retzius cells in segmental ganglia, which then released serotonin to initiate and control all aspects of feeding behavior. In this study, we show that chemosensory or thermal activation of the lip lasting for at least 5 min produces a distinct signal in the cephalic nerves consisting of action potentials of low amplitude. These small amplitude signals are clearly distinguishable from the large action potentials evoked by mechanosensory stimuli applied to the same area of the lip. Both types of sensory stimuli also evoke an increase in the firing frequency of the Retzius cells in segmental ganglia. However, the response recorded in the nerves and the Retzius cells during a maintained stimulus is not constant but decreases with an exponential time course. These results agree with our earlier observations on a semi-intact feeding preparation in which we showed that the firing frequency of the Retzius cell decreased as soon as the leech began to ingest its meal. Therefore, our data provide further evidence suggesting that it is unlikely that heat or chemical cues maintain the Retzius cell in an active state throughout the consummatory phase of feeding.     

A general odorant background affects the coding of pheromone stimulus intermittency in specialist olfactory receptor neurones

In nature the aerial trace of pheromone used by male moths to find a female appears as a train of discontinuous pulses separated by gaps among a complex odorant background constituted of plant volatiles. We investigated the effect of such background odor on behavior and coding of temporal parameters of pheromone pulse trains in the pheromone olfactory receptor neurons of Spodoptera littoralis. Effects of linalool background were tested by measuring walking behavior towards a source of pheromone. While velocity and orientation index did drop when linalool was turned on, both parameters recovered back to pre-background values after 40 s with linalool still present. Photo-ionization detector was used to characterize pulse delivery by our stimulator. The photo-ionization detector signal reached 71% of maximum amplitude at 50 ms pulses and followed the stimulus period at repetition rates up to 10 pulses/s. However, at high pulse rates the concentration of the odorant did not return to base level during inter-pulse intervals. Linalool decreased the intensity and shortened the response of receptor neurons to pulses. High contrast (>10 dB) in firing rate between pulses and inter-pulse intervals was observed for 1 and 4 pulses/s, both with and without background. Significantly more neurons followed the 4 pulses/s pattern when delivered over linalool; at the same time the information content was preserved almost to the control values. Rapid recovery of behavior shows that change of perceived intensity is more important than absolute stimulus intensity. While decreasing the response intensity, background odor preserved the temporal parameters of the specific signal.     

Stimulus-dependent oscillations and evoked potentials in chinchilla auditory cortex

Besides the intensity and frequency of an auditory stimulus, the length of time that precedes the stimulation is an important factor that determines the magnitude of early evoked neural responses in the auditory cortex. Here we used chinchillas to demonstrate that the length of the silent period before the presentation of an auditory stimulus is a critical factor that modifies late oscillatory responses in the auditory cortex. We used tetrodes to record local-field potential (LFP) signals from the left auditory cortex of ten animals while they were stimulated with clicks, tones or noise bursts delivered at different rates and intensity levels. We found that the incidence of oscillatory activity in the auditory cortex of anesthetized chinchillas is dependent on the period of silence before stimulation and on the intensity of the auditory stimulus. In 62.5% of the recordings sites we found stimulus-related oscillations at around 8-20 Hz. Stimulus-induced oscillations were largest and consistent when stimuli were preceded by 5 s of silence and they were absent when preceded by less than 500 ms of silence. These results demonstrate that the period of silence preceding the stimulus presentation and the stimulus intensity are critical factors for the presence of these oscillations.