Latency as a function of intensity in auditory neurons: influences of central processing

Klug, Achim; Khan, Adnan; Burger, R. Michael; Bauer, Eric E.; Hurley, Laura M.; Yang, Lichuan; Grothe, Benedikt; Halvorsen, Michele B.; Park, Thomas J.

doi:10.1016/s0378-5955(00)00146-5

Cited by 73 publications

(76 citation statements)

References 66 publications

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“…1 A). Such a wide range is typical of IC neurons in the free-tailed bat and in other species (Bodenhamer and Pollak, 1981;Klug et al, 2000, Syka et al, 2000. Latency varied with recording depth, such that neurons recorded at shallower depths along the dorsoventral axis of the IC had longer latencies (multiple regression, p Ͻ 0.01; r 2 ϭ 0.24) and also exhibited a greater range of latencies than neurons deeper in the dorsoventral axis (Fig.…”

Section: Serotonin Changes First-spike Latencies Of Ic Neuronsmentioning

confidence: 82%

“…This circuitry creates many of the same latencydependent response characteristics in Mexican free-tailed bats that are observed in other vertebrates. These response characteristics include paradoxical latency shifts, time-intensity trading, and latency-dependent binaural interactions (Kuwada and Yin, 1983;Pollak, 1988;Melssen et al, 1990;Park et al, 1998;Klug et al, 2000). Importantly, the similarities between the IC of free-tailed bats and other mammals extend to the pattern of innervation by serotonergic fibers, which is similar across species (Kaiser and Covey, 1997;Hurley and Thompson, 2001).…”

Section: Methodsmentioning

confidence: 99%

“…However, despite this evidence, there has been little focus within the auditory system or other sensory systems on the specific ways that neuromodulators change latencies and whether these vary for different cell types or occur independently from neuromodulatory effects on response strength. In the experiments described here, we addressed these issues by applying serotonin iontophoretically while recording from single neurons in the inferior colliculus (IC), a nucleus in which the stimulus features that influence latency Fuzessery and Hall, 1996;Barsz et al, 1998;Klug et al, 2000;Galazyuk and Feng, 2001;Faure et al, 2003) and the modulation of response properties by serotonin Pollak, 1999, 2001;Hurley et al, 2002Hurley et al, , 2004 have been well studied. With this approach, we characterized serotonergic effects on latency by (1) quantifying serotonergic effects on the latency and precision of spikes, (2) comparing serotoninevoked changes in latency with changes in spike count and other response properties, and (3) determining the dependence of serotonin-evoked latency shifts on features of the stimulus.…”

Section: Introductionmentioning

confidence: 99%

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Serotonin Shifts First-Spike Latencies of Inferior Colliculus Neurons

Hurley¹,

Pollak²

2005

J. Neurosci.

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Many studies of neuromodulators have focused on changes in the magnitudes of neural responses, but fewer studies have examined neuromodulator effects on response latency. Across sensory systems, response latency is important for encoding not only the temporal structure but also the identity of stimuli. In the auditory system, latency is a fundamental response property that varies with many features of sound, including intensity, frequency, and duration. To determine the extent of neuromodulatory regulation of latency within the inferior colliculus (IC), a midbrain auditory nexus, the effects of iontophoretically applied serotonin on first-spike latencies were characterized in the IC of the Mexican free-tailed bat. Serotonin significantly altered the first-spike latencies in response to tones in 24% of IC neurons, usually increasing, but sometimes decreasing, latency. Serotonin-evoked changes in latency and spike count were not always correlated but sometimes occurred independently within individual neurons. Furthermore, in some neurons, the size of serotonin-evoked latency shifts depended on the frequency or intensity of the stimulus, as reported previously for serotonin-evoked changes in spike count. These results support the general conclusion that changes in latency are an important part of the neuromodulatory repertoire of serotonin within the auditory system and show that serotonin can change latency either in conjunction with broad changes in other aspects of neuronal excitability or in highly specific ways.

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Section: Serotonin Changes First-spike Latencies Of Ic Neuronsmentioning

confidence: 82%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Serotonin Shifts First-Spike Latencies of Inferior Colliculus Neurons

Hurley¹,

Pollak²

2005

J. Neurosci.

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“…This possibility depends on two kinds of timing mechanisms: multisynaptic delay lines that control the arrival times of excitatory and inhibitory inputs at the IC (Haplea et al, 1994;Klug et al, 2000) and integration of these inputs at the cell membrane. These mechanisms allow for the comparison of information from more than one time interval so that the cell does not fire until the entire temporal sequence and the subsequent integration is over.…”

Section: Inhibitory Control Of Temporal Maskingmentioning

confidence: 99%

Temporal Masking Reveals Properties of Sound-Evoked Inhibition in Duration-Tuned Neurons of the Inferior Colliculus

et al. 2003

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The inferior colliculus (IC) is the first place in the central auditory pathway where duration-selective neurons are found. Previous neuropharmacological and electrophysiological studies have shown that they are created there and have led to a conceptual model in which excitatory and inhibitory inputs are offset in time so that the cell fires only when sound duration is such that onset-and offsetevoked excitation coincide; the response is suppressed by inhibition at other durations. We tested predictions from the model using paired tone stimulation and extracellular recording in the IC of the big brown bat, Eptesicus fuscus. Responses to a best duration (BD) tone were used as a probe to examine the strength and time course of inhibition activated by a nonexcitatory (NE) tone of the same frequency but differing in duration. As the relative time between the BD and NE tones was varied, the activity evoked by the BD tone was affected in ways comparable with backward, simultaneous, and forward masking. Responses to the BD tone were completely suppressed at short interstimulus intervals when the BD tone preceded the NE tone. Suppression was also seen when the stimuli temporally overlapped and summed and at intervals when the BD tone followed the NE tone. The results show that duration-selective neurons receive an onsetevoked, inhibitory input that precedes their excitatory input. The period of leading inhibition was correlated with BD and first spike latency. The results suggest how inhibition in the CNS could explain temporal masking phenomena, including backward masking.

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“…In the rat, guinea pig, cat, and bats, the majority of IC neurons have response latencies between 5 and 50 ms (Kitzes et al 1978;Jen and Schlegel 1982;Harrison and Palmer 1984;Langner et al 1987;Park and Pollak 1993;Ehert and Romand 1992;Fitzpatrick et al 1995;Le Beau et al 1996;Lu et al 1997;Ferragamo et al 1998;Klug et al 2000;Syka et al 2000). This range is broader than observed in lower auditory brainstem nuclei (Halpea et al 1994;Klug et al 2000). Several functions have been suggested for this wider range of response latencies in the IC.…”

Section: Introductionmentioning

confidence: 96%

Inhibition Has Little Effect on Response Latencies in the Inferior Colliculus

Fuzessery

Wenstrup

Hall

et al. 2003

JARO - Journal of the Association for Research in Otolaryngolog

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The inferior colliculi of all mammals are characterized by a wide range of first-spike response latencies that can greatly exceed the minimum time required for the transmission of input through the lower brainstem. The mechanisms that account for long response latencies of up to 50 ms are unclear, but one hypothesis is that an early inhibition plays a role in shaping latency. To test this hypothesis, response latencies were measured in the inferior colliculi of the pallid and mustached bats before and during the blockade of GABAa and glycine receptors. The effect of blocking inhibition on response latency was compared under stimulus conditions that produced the shortest latency in the predrug condition. Multibarrel ''piggyback'' electrodes were used to iontophoretically apply bicuculline and strychnine sequentially while recording from single neurons. Predrug latencies ranged from 9 to 26 ms in the pallid bat and from 4 to 17 ms in the mustached bat. Despite large increases in response magnitude and response duration following disinhibition, the blockade of inhibitory receptors had modest effects on response latency. In the pallid bat, blocking GABA receptors produced latency changes that ranged from )3.8 to +0.2 ms, while blocking glycine receptors produced changes from )0.1 to +1.7 ms. Similarly, in the mustached bat, blocking GABA receptors caused changes ranging from )10.3 to +1.4 ms; blocking glycine receptors in the mustached bat caused changes from )3.6 to +1.0 ms. The large change of )10.3 ms was an exception. In both species, the majority of neurons showed changes of <1 ms. We conclude that a fast, early inhibitory input does not appear to play a significant role in shaping the wide range of response latencies present in the inferior colliculi of mustached and pallid bats.

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Latency as a function of intensity in auditory neurons: influences of central processing

Cited by 73 publications

References 66 publications

Serotonin Shifts First-Spike Latencies of Inferior Colliculus Neurons

Serotonin Shifts First-Spike Latencies of Inferior Colliculus Neurons

Temporal Masking Reveals Properties of Sound-Evoked Inhibition in Duration-Tuned Neurons of the Inferior Colliculus

Inhibition Has Little Effect on Response Latencies in the Inferior Colliculus

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