Information content of auditory cortical responses to time-varying acoustic stimuli

The present study explores the issue of cortical coding by spike count and timing using statistical and information theoretic methods. We have shown in previous studies that neurons in the auditory cortex of awake primates have an abundance of sustained discharges that could represent time-varying signals by temporal discharge patterns or mean firing rates. In particular, we found that a subpopulation of neurons can encode rapidly occurring sounds, such as a click train, with discharges that are not synchronized to individual stimulus events, suggesting a temporal-to-rate transformation. We investigated whether there were stimulus-specific temporal patterns embedded in these seemingly random spike times. Furthermore, we quantitatively analyzed the precision of spike timing at stimulus onset and during ongoing acoustic stimulation. The main findings are the following. 1) Temporal and rate codes may operate at separate stimulus domains or encode the same stimulus domain in parallel via different neuronal populations. 2) Spike timing was crucial to encode stimulus periodicity in "synchronized" neurons. 3) "Nonsynchronized" neurons showed little stimulus-specific spike timing information in their responses to time-varying signals. Such responses therefore represent processed (instead of preserved) information in the auditory cortex. And 4) spike timing on the occurrence of acoustic events was more precise at the first event than at successive ones and more precise with sparsely distributed events (longer time intervals between events) than with densely packed events. These results indicate that auditory cortical neurons mark sparse acoustic events (or onsets) with precise spike timing and transform rapidly occurring acoustic events into firing rate-based representations.     

Millisecond-scale differences in neural activity in auditory cortex can drive decisions

Neurons in the auditory cortex can lock to the fine timing of acoustic stimuli with millisecond precision, but it is not known whether this precise spike timing can be used to guide decisions. We used chronically implanted microelectrode pairs to stimulate neurons in the rat auditory cortex directly and found that rats can exploit differences in the timing of cortical activity that are as short as 3 ms to guide decisions.     

Sensitivity of auditory cortical neurons to the locations of leading and lagging sounds

We recorded unit activity in the auditory cortex (fields A1, A2, and PAF) of anesthetized cats while presenting paired clicks with variable locations and interstimulus delays (ISDs). In human listeners, such sounds elicit the precedence effect, in which localization of the lagging sound is impaired at ISDs less, similar10 ms. In the present study, neurons typically responded to the leading stimulus with a brief burst of spikes, followed by suppression lasting 100-200 ms. At an ISD of 20 ms, at which listeners report a distinct lagging sound, only 12% of units showed discrete lagging responses. Long-lasting suppression was found in all sampled cortical fields, for all leading and lagging locations, and at all sound levels. Recordings from awake cats confirmed this long-lasting suppression in the absence of anesthesia, although recovery from suppression was faster in the awake state. Despite the lack of discrete lagging responses at delays of 1-20 ms, the spike patterns of 40% of units varied systematically with ISD, suggesting that many neurons represent lagging sounds implicitly in their temporal firing patterns rather than explicitly in discrete responses. We estimated the amount of location-related information transmitted by spike patterns at delays of 1-16 ms under conditions in which we varied only the leading location or only the lagging location. Consistent with human psychophysical results, transmission of information about the leading location was high at all ISDs. Unlike listeners, however, transmission of information about the lagging location remained low, even at ISDs of 12-16 ms.     

Action potential timing precision in dorsal cochlear nucleus pyramidal cells

Many studies of the dorsal cochlear nucleus (DCN) have focused on the representation of acoustic stimuli in terms of average firing rate. However, recent studies have emphasized the role of spike timing in information encoding. We sought to ascertain whether DCN pyramidal cells might employ similar strategies and to what extent intrinsic excitability regulates spike timing. Gaussian distributed low-pass noise current was injected into pyramidal cells in a brain slice preparation. The shuffled autocorrelation-based analysis was used to compute a correlation index of spike times across trials. The noise causes the cells to fire with temporal precision (SD congruent with 1-2 ms) and high reproducibility. Increasing the coefficient of variation of the noise improved the reproducibility of the spike trains, whereas increasing the firing rate of the neuron decreased the neurons' ability to respond with predictable patterns of spikes. Simulated inhibitory postsynaptic potentials superimposed on the noise stimulus enhanced spike timing for >300 ms, although the enhancement was greatest during the first 100 ms. We also found that populations of pyramidal neurons respond to the same noise stimuli with correlated spike trains, suggesting that ensembles of neurons in the DCN receiving shared input can fire with similar timing. These results support the hypothesis that spike timing can be an important aspect of information coding in the DCN.     

Cortical responses in rats predict perceptual sensitivities to complex sounds

The common assumption that perceptual sensitivities are related to neural representations of sensory stimuli has seldom been directly demonstrated. The authors analyzed the similarity of spike trains evoked by complex sounds in the rat auditory cortex and related cortical responses to performance in an auditory task. Rats initially learned to identify 2 highly different periodic, frequency-modulated sounds and then were tested with increasingly similar sounds. Rats correctly classified most novel sounds; their accuracy was negatively correlated with acoustic similarity. Rats discriminated novel sounds with slower modulation more accurately than sounds with faster modulation. This asymmetry was consistent with similarities in cortical representations of the sounds, demonstrating that perceptual sensitivities to complex sounds can be predicted from the cortical responses they evoke.     

AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli

Information processing in the brain may rely on temporal correlations in spike activity between neurons. Within the olfactory bulb, correlated spiking in output mitral cells could affect the odor code by either binding or amplifying signals from individual odorant receptors. We examined the timing of spike trains in mitral cells of rat olfactory bulb slices. Depolarization of mitral cell pairs elicited spikes that were correlated on a rapid timescale (< or =10 ms) for cells whose primary dendrites projected to the same glomerulus. Correlated spiking was driven by a novel mechanism that depended on electrical coupling at mitral cell primary dendrites; the specific synchronizing signal was a coupled depolarization ( approximately 20 ms) that was mediated by dendritic AMPA autoreceptors. We suggest that glomerulus-specific correlated spiking in mitral cells helps to preserve the fidelity of odor signals that are delivered to the olfactory cortex.     

Peculiarities of inhibition in cat auditory cortex neurons evoked by tonal stimuli of various durations

Summary The extra- and intracellular responses of 262 neurons in A1 to tones of best frequency with durations ranging from 10 ms to 1.2 min were studied acute experiments on ketamine-anesthetized cats. Following the generation of action potentials in response to the tone stimulus, inhibition of both the background and the auditory stimulus-evoked spike activity were observed in 91% of the investigated neurons. The duration of this inhibition corresponded to the stimulus duration. For the remaining neurons (9%) an inhibition of the stimulus-evoked spike activity alone was seen, also corresponding to the stimulus duration. Maximal inhibition of the spike activity occurred for the first 100–200 ms of the inhibitory response (the period which equalled the time of development of an IPSP in a cell). During this period of IPSP development, the membrane resistance of the neuron was reduced to 60–90% of its initial value. Varying the duration of the acoustic signal within a range of 10–200 ms was accompanied by a change in the IPSP duration and inhibition of the spike acitivity of the neuron. Whenever the tone lasted more than 200 ms, the membrane potential of the neuron was restored to the resting potential. However, during this period, the responsiveness of the neuron was lower than that initially observed. Measurement of the membrane resistance during the inhibitory pause that was not accompanied by hyperpolarization produced an index with an average 17% lower than the initial value for 87% of the neurons.The data indicate that inhibition of the spike activity in Al neurons evoked by tone stimuli of various durations is due to the appearance of postsynaptic inhibition on their membrane. It is concluded that the time course of the cortical inhibitory input to neurons is the major factor determining variations in duration of the inhibition of response of auditory cortex neurons to an auditory stimulus.     

Subset of thin spike cortical neurons preserve the peripheral encoding of stimulus onsets

An important question in auditory neuroscience concerns how the neural representation of sound features changes from the periphery to the cortex. Here we focused on the encoding of sound onsets and we used a modeling approach to explore the degree to which auditory cortical neurons follow a similar envelope integration mechanism found at the auditory periphery. Our "forward" model was able to predict relatively accurately the timing of first spikes evoked by natural communication calls in the auditory cortex of awake, head-restrained mice, but only for a subset of cortical neurons. These neurons were systematically different in their encoding of the calls, exhibiting less call selectivity, shorter latency, greater precision, and more transient spiking compared with the same factors of their poorly predicted counterparts. Importantly, neurons that fell into this best-predicted group all had thin spike waveforms, suggestive of suspected interneurons conveying feedforward inhibition. Indeed, our population of call-excited thin spike neurons had significantly higher spontaneous rates and larger frequency tuning bandwidths than those of thick spike neurons. Thus the fidelity of our model's first spike predictions segregated neurons into one earlier responding subset, potentially dominated by suspected interneurons, which preserved a peripheral mechanism for encoding sound onsets and another longer latency subset that reflected higher, likely centrally constructed nonlinearities. These results therefore provide support for the hypothesis that physiologically distinct subclasses of neurons in the auditory cortex may contribute hierarchically to the representation of natural stimuli.     

Timing of sound-evoked potentials and spike responses in the inferior colliculus of awake bats

Neurons in the inferior colliculus (IC), one of the major integrative centers of the auditory system, process acoustic information converging from almost all nuclei of the auditory brain stem. During this integration, excitatory and inhibitory inputs arrive to auditory neurons at different time delays. Result of this integration determines timing of IC neuron firing. In the mammalian IC, the range of the first spike latencies is very large (5-50 ms). At present, a contribution of excitatory and inhibitory inputs in controlling neurons' firing in the IC is still under debate. In the present study we assess the role of excitation and inhibition in determining first spike response latency in the IC. Postsynaptic responses were recorded to pure tones presented at neuron's characteristic frequency or to downward frequency modulated sweeps in awake bats. There are three main results emerging from the present study: (1) the most common response pattern in the IC is hyperpolarization followed by depolarization followed by hyperpolarization, (2) latencies of depolarizing or hyperpolarizing responses to tonal stimuli are short (3-7 ms) whereas the first spike latencies may vary to a great extent (4-26 ms) from one neuron to another, and (3) high threshold hyperpolarization preceded long latency spikes in IC neurons exhibiting paradoxical latency shift. Our data also show that the onset hyperpolarizing potentials in the IC have very small jitter (<100 mus) across repeated stimulus presentations. The results of this study suggest that inhibition, arriving earlier than excitation, may play a role as a mechanism for delaying the first spike latency in IC neurons.     

Responses of auditory cortical neurons to pairs of sounds: correlates of fusion and localization

When two brief sounds arrive at a listener's ears nearly simultaneously from different directions, localization of the sounds is described by "the precedence effect." At inter-stimulus delays (ISDs) <5 ms, listeners typically report hearing not two sounds but a single fused sound. The reported location of the fused image depends on the ISD. At ISDs of 1-4 ms, listeners point near the leading source (localization dominance). As the ISD is decreased from 0.8 to 0 ms, the fused image shifts toward a location midway between the two sources (summing localization). When an inter-stimulus level difference (ISLD) is imposed, judgements shift toward the more intense source. Spatial hearing, including the precedence effect, is thought to depend on the auditory cortex. Therefore we tested the hypothesis that the activity of cortical neurons signals the perceived location of fused pairs of sounds. We recorded the unit responses of cortical neurons in areas A1 and A2 of anesthetized cats. Single broadband clicks were presented from various frontal locations. Paired clicks were presented with various ISDs and ISLDs from two loudspeakers located 50 degrees to the left and right of midline. Units typically responded to single clicks or paired clicks with a single burst of spikes. Artificial neural networks were trained to recognize the spike patterns elicited by single clicks from various locations. The trained networks were then used to identify the locations signaled by unit responses to paired clicks. At ISDs of 1-4 ms, unit responses typically signaled locations near that of the leading source in agreement with localization dominance. Nonetheless the responses generally exhibited a substantial undershoot; this finding, too, accorded with psychophysical measurements. As the ISD was decreased from ~0.4 to 0 ms, network estimates typically shifted from the leading location toward the midline in agreement with summing localization. Furthermore a superposed ISLD shifted network estimates toward the more intense source, reaching an asymptote at an ISLD of 15-20 dB. To allow quantitative comparison of our physiological findings to psychophysical results, we performed human psychophysical experiments and made acoustical measurements from the ears of cats and humans. After accounting for the difference in head size between cats and humans, the responses of cortical units usually agreed with the responses of human listeners, although a sizable minority of units defied psychophysical expectations.     

Auditory evoked visual awareness following sudden ocular blindness: an EEG and TMS investigation

Neurophysiological and neuroanatomical studies have provoked controversy about whether the visual cortex may be more modifiable than previously believed. Auditory processing is enhanced in blind compared to sighted people, and the enhancement might reflect encroachment of auditory transmission onto visual cortex. To address this issue, we recorded the auditory event-related potentials (ERPs) correlated with auditory related paradoxical visual awareness in a subject with traumatic total late-onset blindness. We found that (1) there was auditory related brain activity over the occipital visual scalp regions starting from a very early stage (< 80 ms) and (2) this occipital activity was significantly different between “visually aware” and “visually unaware” responses in the P1 (40–80 ms) component following meaningful stimuli. There was also a significant difference between responses with and without visual awareness in the N1 (100–120 ms) component following either tones or meaningful stimuli. The phosphenes accompanying auditory stimuli in the ERP experiment were always perceived to be directly in front of the subject and this was reproduced by transcranial magnetic stimulation over the blind primary visual cortex and by sudden sounds delivered to the side or behind the subject. The TMS induced phosphenes were restricted to the central part of the space and were, at least qualitatively, the same as those induced by sounds. The results are clear evidence that human perceptual functions can be reorganized after sudden, late-onset, total ocular blindness.     

Roles of axonal sodium channels in precise auditory time coding at nucleus magnocellularis of the chick

How the axonal distribution of Na⁺ channels affects the precision of spike timing is not well understood. We addressed this question in auditory relay neurons of the avian nucleus magnocellularis. These neurons encode and convey information about the fine structure of sounds to which they are tuned by generating precisely timed action potentials in response to synaptic inputs. Patterns of synaptic inputs differ as a function of tuning. A small number of large inputs innervate high- and middle-frequency neurons, while a large number of small inputs innervate low-frequency neurons. We found that the distribution and density of Na⁺ channels in the axon initial segments varied with the synaptic inputs, and were distinct in the low-frequency neurons. Low-frequency neurons had a higher density of Na⁺ channels within a longer axonal stretch, and showed a larger spike amplitude and whole-cell Na⁺ current than high/middle-frequency neurons. Computer simulations revealed that for low-frequency neurons, a large number of Na⁺ channels were crucial for preserving spike timing because it overcame Na⁺ current inactivation and K⁺ current activation during compound EPSPs evoked by converging small inputs. In contrast, fewer channels were sufficient to generate a spike with high precision in response to an EPSP induced by a single massive input in the high/middle-frequency neurons. Thus the axonal Na⁺ channel distribution is effectively coupled with synaptic inputs, allowing these neurons to convey auditory information in the timing of firing.     

Hierarchical and asymmetric temporal sensitivity in human auditory cortices

Lateralization of function in auditory cortex has remained a persistent puzzle. Previous studies using signals with differing spectrotemporal characteristics support a model in which the left hemisphere is more sensitive to temporal and the right more sensitive to spectral stimulus attributes. Here we use single-trial sparse-acquisition fMRI and a stimulus with parametrically varying segmental structure affecting primarily temporal properties. We show that both left and right auditory cortices are remarkably sensitive to temporal structure. Crucially, beyond bilateral sensitivity to timing information, we uncover two functionally significant interactions. First, local spectrotemporal signal structure is differentially processed in the superior temporal gyrus. Second, lateralized responses emerge in the higher-order superior temporal sulcus, where more slowly modulated signals preferentially drive the right hemisphere. The data support a model in which sounds are analyzed on two distinct timescales, 25-50 ms and 200-300 ms.     

Unbalanced synaptic inhibition can create intensity-tuned auditory cortex neurons

Intensity-tuned auditory cortex neurons have spike rates that are nonmonotonic functions of sound intensity: their spike rate initially increases and peaks as sound intensity is increased, then decreases as sound intensity is further increased. They are either "unbalanced," receiving disproportionally large synaptic inhibition at high sound intensities; or "balanced," receiving intensity-tuned synaptic excitation and identically tuned synaptic inhibition which neither creates enhances nor creates intensity-tuning. It has remained unknown if the synaptic inhibition received by unbalanced neurons enhances intensity-tuning already present in the synaptic excitation, or if it creates intensity-tuning that is not present in the synaptic excitation. Here we show, using in vivo whole cell recordings in pentobarbital-anesthetized rats, that in some unbalanced intensity-tuned auditory cortex neurons synaptic inhibition enhances the intensity-tuning; while in others it actually creates the intensity-tuning. The lack of balance between synaptic excitation and inhibition was not always apparent in their peak amplitudes, but could sometimes be revealed only by considering their relative timing. Since synaptic inhibition is essentially cortical in origin, the unbalanced neurons in which inhibition creates intensity-tuning provide examples of auditory feature-selectivity arising de novo at the auditory cortex.     

Neural representations of temporally asymmetric stimuli in the auditory cortex of awake primates

The representation of rapid acoustic transients by the auditory cortex is a fundamental issue that is still unresolved. Auditory cortical neurons have been shown to be limited in their stimulus-synchronized responses, yet the perceptual performances of humans and animals in discriminating temporal variations in complex sounds are better than what existing neurophysiological data would predict. This study investigated the neural representation of temporally asymmetric stimuli in the primary auditory cortex of awake marmoset monkeys. The stimuli, ramped and damped sinusoids, were systematically manipulated (by means of half-life of the exponential envelope) within a cortical neuron's presumed temporal integration window. The main findings of this study are as follows: 1) temporal asymmetry in ramped and damped sinusoids with a short period (25 ms) was clearly reflected by average discharge rate but not necessarily by temporal discharge patterns of auditory cortical neurons. There was considerable response specificity to these stimuli such that some neurons were strongly responsive to a ramped sinusoid but almost completely unresponsive to its damped counterpart or vice versa. Of 181 neurons studied, 140 (77%) showed significant response asymmetry in at least one of the tested half-life values of the exponential envelope. Forty-six neurons showed significant response asymmetry over all half-lives tested. Sustained firing, commonly observed under awake conditions, contributed to greater response asymmetry than that of onset responses in many neurons. 2) A greater proportion of the neurons (32/46) that exhibited significant overall response asymmetry showed stronger responses to the ramped sinusoids than to the damped sinusoids, possibly contributing to the difference in the perceived loudness between these two classes of sounds. 3) The asymmetry preference of a neuron to ramped or damped sinusoids did not appear to be correlated with its characteristic frequency or minimum response latency, suggesting that this is a general phenomenon that exists across populations of cortical neurons. Moreover, the intensity of the stimuli did not have significant effects on the measure of the asymmetry preference based on discharge rate. 4) A population measure of response preference, based on discharge rate, of cortical neurons to the temporally asymmetric stimuli was qualitatively similar to the performance of human listeners in discriminating ramped versus damped sinusoids at different half-life values. These findings suggest that rapid acoustic transients embedded in complex sounds can be represented by discharge rates of cortical neurons instead of or in the absence of stimulus-synchronized discharges.     

Effects of inhibitory timing on contrast enhancement in auditory circuits in crickets (Teleogryllus oceanicus)

In crickets (Teleogryllus oceanicus), the paired auditory interneuron Omega Neuron 1 (ON1) responds to sounds with frequencies in the range from 3 to 40 kHz. The neuron is tuned to frequencies similar to that of conspecific songs (4.5 kHz), but its latency is longest for these same frequencies by a margin of 5-10 ms. Each ON1 is strongly excited by input from the ipsilateral ear and inhibits contralateral auditory neurons that are excited by the contralateral ear, including the interneurons ascending neurons 1 and 2 (AN1 and AN2). We investigated the functional consequences of ON1's long latency to cricket-like sound and the resulting delay in inhibition of AN1 and AN2. Using dichotic stimuli, we controlled the timing of contralateral inhibition of the ANs relative to their excitation by ipsilateral stimuli. Advancing the stimulus to the ear driving ON1 relative to that driving the ANs "subtracted" ON1's additional latency to 4.5 kHz. This had little effect on the spike counts of AN1 and AN2. The response latencies of these neurons, however, increased markedly. This is because in the absence of a delay in ON1's response, inhibition arrived at AN1 and AN2 early enough to abolish the first spikes in their responses. This also increased the variability of AN1 latency. This suggests that one possible function of the delay in ON1's response may be to protect the precise timing of the onset of response in the contralateral AN1, thus preserving interaural difference in response latency as a reliable potential cue for sound localization. Hyperpolarizing ON1 removed all detectable contralateral inhibition of AN1 and AN2, suggesting that ON1 is the main, if not the only, source of contralateral inhibition.     

Processing of low-probability sounds by cortical neurons

The ability to detect rare auditory events can be critical for survival. We report here that neurons in cat primary auditory cortex (A1) responded more strongly to a rarely presented sound than to the same sound when it was common. For the rare stimuli, we used both frequency and amplitude deviants. Moreover, some A1 neurons showed hyperacuity for frequency deviants--a frequency resolution one order of magnitude better than receptive field widths in A1. In contrast, auditory thalamic neurons were insensitive to the probability of frequency deviants. These phenomena resulted from stimulus-specific adaptation in A1, which may be a single-neuron correlate of an extensively studied cortical potential--mismatch negativity--that is evoked by rare sounds. Our results thus indicate that A1 neurons, in addition to processing the acoustic features of sounds, may also be involved in sensory memory and novelty detection.     

Processing of modulated sounds in the zebra finch auditory midbrain: responses to noise, frequency sweeps, and sinusoidal amplitude modulations

The avian auditory midbrain nucleus, the mesencephalicus lateralis, dorsalis (MLd), is the first auditory processing stage in which multiple parallel inputs converge, and it provides the input to the auditory thalamus. We studied the responses of single MLd neurons to four types of modulated sounds: 1) white noise; 2) band-limited noise; 3) frequency modulated (FM) sweeps, and 4) sinusoidally amplitude-modulated tones (SAM) in adult male zebra finches. Responses were compared with the responses of the same neurons to pure tones in terms of temporal response patterns, thresholds, characteristic frequencies, frequency tuning bandwidths, tuning sharpness, and spike rate/intensity relationships. Most neurons responded well to noise. More than one-half of the neurons responded selectively to particular portions of the noise, suggesting that, unlike forebrain neurons, many MLd neurons can encode specific acoustic components of highly modulated sounds such as noise. Selectivity for FM sweep direction was found in only 13% of cells that responded to sweeps. Those cells also showed asymmetric tuning curves, suggesting that asymmetric inhibition plays a role in FM directional selectivity. Responses to SAM showed that MLd neurons code temporal modulation rates using both spike rate and synchronization. Nearly all cells showed low-pass or band-pass filtering properties for SAM. Best modulation frequencies matched the temporal modulations in zebra finch song. Results suggest that auditory midbrain neurons are well suited for encoding a wide range of complex sounds with a high degree of temporal accuracy rather than selectively responding to only some sounds.     

An analysis of penicillin-induced generalized spike and wave discharges using simultaneous recordings of cortical and thalamic single neurons

To study the relationship between cortical and thalamic single-neuron activity during spike and wave (SW) discharge of feline generalized penicillin epilepsy (FGPE), extracellular single-unit and local electroencephalogram (EEG) activity were recorded simultaneously from pairs of neurons, one located in the cortex of the middle suprasylvian gyrus (MSS), the other in the dorsal thalamic nuclei (n. lateralis posterior or pulvinar). These two areas are anatomically and functionally closely interrelated. Computer-generated EEG averages and histograms of single-unit activity triggered by either peaks of cortical or thalamic EEG transients or by cortical or thalamic action potentials (aps) showed that cortical neurons in the MSS fired at the time of the spike of the SW complex, while at the time of the wave they became silent. Two populations of thalamic neurons also fired maximally during the spike of SW discharge, but they differed in the precise timing of their firing in relation to that of the simultaneously recorded cortical neuron. The first group of thalamic neurons tended to fire 5-45 ms before the cortical neuron. Of these 28 neurons, 9 were antidromically and 2 orthodromically activated by cortical stimulation. The neurons of the second group tended to fire 0-45 ms after the cortical neuron. Cortical stimulation activated 15 of these 19 neurons orthodromically and 2 antidromically. A third and smaller population of thalamic neurons (n = 8) increased its firing probability during the wave of the SW complex and decreased it during the spike. In 74% of the pairs of neurons the cyclic alternation of excitation and "inhibition" associated with SW activity appeared in the cortex by 1-3 cycles earlier than in the thalamus. This was most common when the thalamic neuron of the pair reached its peak firing probability before the simultaneously recorded cortical neuron. In 11 pairs of neurons the same rhythmic alternation of excitation and "inhibition" of neuronal firing was seen in both the cortex and thalamus during SW discharges evoked by single-shock stimulation of nucleus centralis medialis. These data demonstrate that both cortical and thalamic neurons participate in the SW firing pattern of FGPE by undergoing periods of mutually phase-locked cyclic alternations of excitation and "inhibition" at the frequency of the EEG SW rhythm. Although the initial steps leading to generalized SW discharge in FGPE take place in the cortex, the thalamus soon becomes entrained in the SW rhythm.(ABSTRACT TRUNCATED AT 400 WORDS)