Abstract:Duration-tuned neurons (DTNs) in the mammalian inferior colliculus (IC) arise from a combination of excitatory and inhibitory synaptic inputs. Previous research has shown that the inhibition responsible for creating DTNs has a shorter latency than that of excitation and lasts longer than the stimulus duration. We used monotic and dichotic paired tone stimulation and recorded responses of DTNs from the IC of the bat to assess the relative contributions of each ear in forming duration-tuned circuits. The stimulu… Show more
“…D: the scatterplot is analogous to that in A, but the analysis interval is limited to the first 100 ms of the response, and only durations of 100 ms or greater (n ϭ 4) are discriminated, which shifts both chance and the statistical criterion to larger values, as indicated by the gray boxes. E and F obey the same conventions as B and C. 2011; Mora and Kössl 2004;Pinheiro et al 1991;Pollak and Schuller 1981;Sayegh et al 2011Sayegh et al , 2014. However, only a handful of studies focused on duration coding involved mammalian species that are not bioacoustically specialized for echolocation.…”
The temporal coherence of amplitude fluctuations is a critical cue for segmentation of complex auditory scenes. The auditory system must accurately demarcate the onsets and offsets of acoustic signals. We explored how and how well the timing of onsets and offsets of gated tones are encoded by auditory cortical neurons in awake rhesus macaques. Temporal features of this representation were isolated by presenting otherwise identical pure tones of differing durations. Cortical response patterns were diverse, including selective encoding of onset and offset transients, tonic firing, and sustained suppression. Spike train classification methods revealed that many neurons robustly encoded tone duration despite substantial diversity in the encoding process. Excellent discrimination performance was achieved by neurons whose responses were primarily phasic at tone offset and by those that responded robustly while the tone persisted. Although diverse cortical response patterns converged on effective duration discrimination, this diversity significantly constrained the utility of decoding models referenced to a spiking pattern averaged across all responses or averaged within the same response category. Using maximum likelihood-based decoding models, we demonstrated that the spike train recorded in a single trial could support direct estimation of stimulus onset and offset. Comparisons between different decoding models established the substantial contribution of bursts of activity at sound onset and offset to demarcating the temporal boundaries of gated tones. Our results indicate that relatively few neurons suffice to provide temporally precise estimates of such auditory "edges," particularly for models that assume and exploit the heterogeneity of neural responses in awake cortex.
“…D: the scatterplot is analogous to that in A, but the analysis interval is limited to the first 100 ms of the response, and only durations of 100 ms or greater (n ϭ 4) are discriminated, which shifts both chance and the statistical criterion to larger values, as indicated by the gray boxes. E and F obey the same conventions as B and C. 2011; Mora and Kössl 2004;Pinheiro et al 1991;Pollak and Schuller 1981;Sayegh et al 2011Sayegh et al , 2014. However, only a handful of studies focused on duration coding involved mammalian species that are not bioacoustically specialized for echolocation.…”
The temporal coherence of amplitude fluctuations is a critical cue for segmentation of complex auditory scenes. The auditory system must accurately demarcate the onsets and offsets of acoustic signals. We explored how and how well the timing of onsets and offsets of gated tones are encoded by auditory cortical neurons in awake rhesus macaques. Temporal features of this representation were isolated by presenting otherwise identical pure tones of differing durations. Cortical response patterns were diverse, including selective encoding of onset and offset transients, tonic firing, and sustained suppression. Spike train classification methods revealed that many neurons robustly encoded tone duration despite substantial diversity in the encoding process. Excellent discrimination performance was achieved by neurons whose responses were primarily phasic at tone offset and by those that responded robustly while the tone persisted. Although diverse cortical response patterns converged on effective duration discrimination, this diversity significantly constrained the utility of decoding models referenced to a spiking pattern averaged across all responses or averaged within the same response category. Using maximum likelihood-based decoding models, we demonstrated that the spike train recorded in a single trial could support direct estimation of stimulus onset and offset. Comparisons between different decoding models established the substantial contribution of bursts of activity at sound onset and offset to demarcating the temporal boundaries of gated tones. Our results indicate that relatively few neurons suffice to provide temporally precise estimates of such auditory "edges," particularly for models that assume and exploit the heterogeneity of neural responses in awake cortex.
“…To date, research on auditory DTNs has focused primarily on the neural mechanisms that create their temporally selective responses Ehrlich et al 1997;Fuzessery and Hall 1999;Hooper et al 2002;Faure et al 2003;Jen and Wu 2006;Aubie et al 2009Aubie et al , 2012Sayegh et al 2012Sayegh et al , 2014 and on the stability (tolerance) of duration tuning with changes in signal amplitude (Zhou and Jen 2001;Mora and Kössl 2004;Fremouw et al 2005). We know that duration tuning is disrupted or abolished by blocking neural inhibition in the IC, which also suggests that duration tuning originates there Faure et al 2003;Leary et al 2008).…”
Neurons throughout the mammalian central auditory pathway respond selectively to stimulus frequency and amplitude, and some are also selective for stimulus duration. First found in the auditory midbrain or inferior colliculus (IC), these duration-tuned neurons (DTNs) provide a potential neural mechanism for encoding temporal features of sound. In this study, we investigated how having an additional neural response filter, one selective to the duration of an auditory stimulus, influences frequency tuning and neural organization by recording single-unit responses and measuring the dorsal-ventral position and spectral-temporal tuning properties of auditory DTNs from the IC of the awake big brown bat (Eptesicus fuscus). Like other IC neurons, DTNs were tonotopically organized and had either V-shaped, U-shaped, or O-shaped frequency tuning curves (excitatory frequency response areas). We hypothesized there would be an interaction between frequency and duration tuning in DTNs, as electrical engineering theory for resonant filters dictates a trade-off in spectral-temporal resolution: sharp tuning in the frequency domain results in poorer resolution in the time domain and vice versa. While the IC is a more complex signal analyzer than an electrical filter, a similar operational trade-off could exist in the responses of DTNs. Our data revealed two patterns of spectro-temporal sensitivity and spatial organization within the IC: DTNs with sharp frequency tuning and broad duration tuning were located in the dorsal IC, whereas cells with wide spectral tuning and narrow temporal tuning were found in the ventral IC.
“…Measuring onset and offset of inhibition with spike counts and latencies. We measured the duration and latency of the inhibition evoked by the NE tone by observing the time points when the BD tone-evoked spike count became suppressed and/or altered in latency, using the same criteria as Sayegh et al (2014). To measure the time course of the inhibition evoked by the NE tone, we first quantified the .…”
Section: Methodsmentioning
confidence: 99%
“…Using three criteria, we compared baseline responses with those obtained at each ISI to determine when spike counts or latencies were altered by NE toneevoked inhibition. As in our previous studies with paired-tone stimulation, we used a combination of detection criteria to measure the time course of inhibition evoked by the NE tone (Faure et al 2003;Sayegh et al 2012Sayegh et al , 2014. We used a 50% change in the evoked spike count as the initial criterion to delineate the time points for the onset and offset of spike suppression.…”
Section: Methodsmentioning
confidence: 99%
“…The final values of T 1 and T 2 were chosen to be those that were most sensitive in capturing the time course of the suppressed response evoked by the NE tone with a spike count and/or spike latency criterion. The use of spike counts or spike latencies (or both) to quantify changes in a neuron's responsiveness has previously been validated (Faure et al 2003;Sayegh et al 2012Sayegh et al , 2014. In cases in which cells responded with only a single spike per stimulus [i.e., baseline first spike latency (L first ) ϭ baseline last spike latency (L last )], a change in spike count was typically used for selecting T 1 and T 2 because this criterion was more accurate in reflecting the time course of the evoked inhibition.…”
Inhibition plays an important role in creating the temporal response properties of duration-tuned neurons (DTNs) in the mammalian inferior colliculus (IC). Neurophysiological and computational studies indicate that duration selectivity in the IC is created through the convergence of excitatory and inhibitory synaptic inputs offset in time. We used paired-tone stimulation and extracellular recording to measure the frequency tuning of the inhibition acting on DTNs in the IC of the big brown bat (). We stimulated DTNs with pairs of tones differing in duration, onset time, and frequency. The onset time of a short, best-duration (BD), probe tone set to the best excitatory frequency (BEF) was varied relative to the onset of a longer-duration, nonexcitatory (NE) tone whose frequency was varied. When the NE tone frequency was near or within the cell's excitatory bandwidth (eBW), BD tone-evoked spikes were suppressed by an onset-evoked inhibition. The onset of the spike suppression was independent of stimulus frequency, but both the offset and duration of the suppression decreased as the NE tone frequency departed from the BEF. We measured the inhibitory frequency response area, best inhibitory frequency (BIF), and inhibitory bandwidth (iBW) of each cell. We found that the BIF closely matched the BEF, but the iBW was broader and usually overlapped the eBW measured from the same cell. These data suggest that temporal selectivity of midbrain DTNs is created and preserved by having cells receive an onset-evoked, constant-latency, broadband inhibition that largely overlaps the cell's excitatory receptive field. We conclude by discussing possible neural sources of the inhibition. Duration-tuned neurons (DTNs) arise from temporally offset excitatory and inhibitory synaptic inputs. We used single-unit recording and paired-tone stimulation to measure the spectral tuning of the inhibitory inputs to DTNs. The onset of inhibition was independent of stimulus frequency; the offset and duration of inhibition systematically decreased as the stimulus departed from the cell's best excitatory frequency. Best inhibitory frequencies matched best excitatory frequencies; however, inhibitory bandwidths were more broadly tuned than excitatory bandwidths.
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