Neuronal activation times to simple, complex, and natural sounds in cat primary and nonprimary auditory cortex

Centre for Brain and Mind, Department of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, University of Western Ontario, London, Ontario, Canada.
Journal of Neurophysiology (Impact Factor: 2.89). 06/2011; 106(3):1166-78. DOI: 10.1152/jn.00940.2010
Source: PubMed


Interactions between living organisms and the environment are commonly regulated by accurate and timely processing of sensory signals. Hence, behavioral response engagement by an organism is typically constrained by the arrival time of sensory information to the brain. While psychophysical response latencies to acoustic information have been investigated, little is known about how variations in neuronal response time relate to sensory signal characteristics. Consequently, the primary objective of the present investigation was to determine the pattern of neuronal activation induced by simple (pure tones), complex (noise bursts and frequency modulated sweeps), and natural (conspecific vocalizations) acoustic signals of different durations in cat auditory cortex. Our analysis revealed three major cortical response characteristics. First, latency measures systematically increase in an antero-dorsal to postero-ventral direction among regions of auditory cortex. Second, complex acoustic stimuli reliably provoke faster neuronal response engagement than simple stimuli. Third, variations in neuronal response time induced by changes in stimulus duration are dependent on acoustic spectral features. Collectively, these results demonstrate that acoustic signals, regardless of complexity, induce a directional pattern of activation in auditory cortex.

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    • "The mean latencies of tone-evoked excitatory responses in the PU and GP neurons (23.1 and 28.2 ms) compare favorably with the auditory mean initial onset latencies reported by other investigators (Bordi and LeDoux 1992; Bordi et al. 1993; Chudler et al. 1995), but this is obviously longer than the latency seen in the cat's A1 neurons (10.9 ms; Carrasco and Lomber 2011) and medial geniculate body neurons (12–18 ms; "
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    ABSTRACT: Several decades of research have provided evidence that the basal ganglia are closely involved in motor processes. Recent clinical, electrophysiological, behavioral data have revealed that the basal ganglia also receive afferent input from the auditory system, but the detailed auditory response characteristics have not yet reported. The present study aimed to reveal the acoustic response properties of neurons in parts of the basal ganglia. We recorded single-unit activities from the putamen (PU) and globus pallidus (GP) of awake cats passively listening to pure-tones, click-trains and natural sounds. Our major findings are: 1) Responses in both PU and GP neurons were elicited by pure-tone stimuli, while PU neurons had lower intensity thresholds, shorter response latencies, shorter excitatory duration and larger response magnitudes than GP neurons. 2) Some GP neurons showed a suppressive response lasting throughout the stimulus period. 3) Both PU and GP had a low ability to follow the periodically repeated click stimuli. Most of neurons only showed a phasic response at the stimulus onset and offset. 4) In response to natural sounds, PU also showed a stronger magnitude and shorter duration of excitatory response than GP. The selectivity for natural sounds was low in both nuclei. 5) Non-biological environmental sounds were more efficient to evoke neural responses in PU and GP than the vocalizations of con-species and other species. Our results provide insights into how acoustic signals are processed in the basal ganglia and revealed the distinction of PU and GP in sensory representation.
    Journal of Neurophysiology 02/2014; 111(10). DOI:10.1152/jn.00830.2013 · 2.89 Impact Factor
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    • "Analysis of neural response latency has been useful in developing models of visual cortical function [29], [30]. Recently, neural latency was also used to reveal the auditory processing stream in cats [31] and primates [32]. In anesthetized rats, some previous studies reported that the mean onset latency was typically longer in PAF than in A1 [5], [7], and others reported that AAF neurons exhibit shorter response latencies than A1 neurons [13]. "
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    ABSTRACT: Cortical representation of time-varying features of acoustic signals is a fundamental issue of acoustic processing remaining unresolved. The rat is a widely used animal model for auditory cortical processing. Though some electrophysiological studies have investigated the neural responses to temporal repetitive sounds in the auditory cortex (AC) of rats, most of them were conducted under anesthetized condition. Recently, it has been shown that anesthesia could significantly alter the temporal patterns of neural response. For this reason, we systematically examined the single-unit neural responses to click-trains in the core region of rat AC under awake condition. Consistent with the reports on anesthetized rats, we confirmed the existence of characteristic tonotopic organizations, which were used to divide the AC into anterior auditory field (AAF), primary auditory cortex (A1) and posterior auditory field (PAF). We further found that the neuron's capability to synchronize to the temporal repetitive stimuli progressively decreased along the anterior-to-posterior direction of AC. The median of maximum synchronization rate was 64, 32 and 16 Hz in AAF, A1 and PAF, respectively. On the other hand, the percentage of neurons, which showed non-synchronized responses and could represent the stimulus repetition rate by the mean firing rate, increased from 7% in AAF and A1 to 20% in PAF. These results suggest that the temporal resolution of acoustic processing gradually increases from the anterior to posterior part of AC, and thus there may be a hierarchical stream along this direction of rat AC.
    PLoS ONE 05/2013; 8(5):e64288. DOI:10.1371/journal.pone.0064288 · 3.23 Impact Factor
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    ABSTRACT: Topographically organized maps of the sensory receptor epithelia are regarded as cornerstones of cortical organization as well as valuable readouts of diverse biological processes ranging from evolution to neural plasticity. However, maps are most often derived from multiunit activity recorded in the thalamic input layers of anesthetized animals using near-threshold stimuli. Less distinct topography has been described by studies that deviated from the formula above, which brings into question the generality of the principle. Here, we explicitly compared the strength of tonotopic organization at various depths within core and belt regions of the auditory cortex using electrophysiological measurements ranging from single units to delta-band local field potentials (LFP) in the awake and anesthetized mouse. Unit recordings in the middle cortical layers revealed a precise tonotopic organization in core, but not belt, regions of auditory cortex that was similarly robust in awake and anesthetized conditions. In core fields, tonotopy was degraded outside the middle layers or when LFP signals were substituted for unit activity, due to an increasing proportion of recording sites with irregular tuning for pure tones. However, restricting our analysis to clearly defined receptive fields revealed an equivalent tonotopic organization in all layers of the cortical column and for LFP activity ranging from gamma to theta bands. Thus, core fields represent a transition between topographically organized simple receptive field arrangements that extend throughout all layers of the cortical column and the emergence of nontonotopic representations outside the input layers that are further elaborated in the belt fields.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 07/2012; 32(27):9159-72. DOI:10.1523/JNEUROSCI.0065-12.2012 · 6.34 Impact Factor
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