GABAergic Disinhibition Affects Responses of Bat Inferior Collicular Neurons to Temporally Patterned Sound Pulses

1998 ◽  
Vol 79 (5) ◽  
pp. 2303-2315 ◽  
Author(s):  
Yong Lu ◽  
Philip H.-S. Jen ◽  
Min Wu

Lu, Yong, Philip H.-S. Jen, and Min Wu. GABAergic disinhibition affects responses of bat inferior collicular neurons to temporally patterned sound pulses. J. Neurophysiol. 79: 2303–2315, 1998. Using the big brown bat, Eptesicus fuscus, as a model mammalian auditory system, we studied the effect of GABAergic disinhibition by bicuculline on the responses of inferior collicular (IC) neurons to temporally patterned trains of sound pulses delivered at different pulse repetition rates (PRRs) under free-field stimulation conditions. All 66 neurons isolated from eight bats either discharged one to two impulses (phasic on responders, n = 41, 62%), three to eight impulses (phasic bursters, n = 19, 29%), or many impulses throughout the entire duration of the stimulus (tonicresponders, n = 6, 9%). Whereas 50 neurons responded vigorously to frequency-modulated (FM) pulses, 16 responded poorly ornot at all to FM pulses. Bicuculline application increased the number of impulses of all 66 neurons in response to 4 ms pulses by 15–1,425%. The application also changed most phasic on responders into phasic bursters or tonic responders, resulting in 12 (18%) phasic on responders, 34 (52%) phasic bursters, and 20 (30%) tonic responders. Response latencies of these neurons were either shortened ( n = 25, 38%) by 0.5–6.0 ms, lengthened ( n = 9, 14%) by 0.5–2.5 ms or not changed ( n = 32, 48%) on bicuculline application. Each neuron had a highest response repetition rate beyond which the neuron failed to respond. Bicuculline application increased the highest response repetition rates of 62 (94%) neurons studied. The application also increased the highest 100% pulse-locking repetition rates of 21 (32%) neurons and facilitated 27 (41%) neurons in response to more pulses at the same PRR than predrug conditions. According to average rate-based modulation transfer functions (average rate MTFs), all 66 neurons had low-pass filtering characteristics both before and after bicuculline application. According to total discharge rate-based modulation transfer functions (total rate MTFs), filtering characteristics of these neurons can be described as band-pass ( n = 52, 79%), low-pass ( n = 12, 18%), or high-pass ( n = 2, 3%) before bicuculline application. Bicuculline application changed the filtering characteristics of 14 (21%) neurons. According to synchronization coefficient-based modulation transfer functions, filtering characteristics of these neurons can be described as low-pass ( n = 41, 62%), all-pass ( n = 11, 17%), band-suppression ( n = 7, 10.5%), and band-suppression–band-pass filters ( n = 7, 10.5%). Bicuculline application changed filtering characteristics of 19 (29%) neurons.

2006 ◽  
Vol 96 (5) ◽  
pp. 2388-2398 ◽  
Author(s):  
Ranjan Batra

Fluctuations in the amplitude of a sound play an important role in our perception of pitch and acoustic space, but their neural analysis has not been fully elucidated. The ventral nucleus of the lateral lemniscus (VNLL) has been implicated in the processing of such temporal features of a sound. This study examines responses of neurons in the VNLL of unanesthetized rabbits to sinusoidally amplitude modulated tones, a type of stimulus that has often been used to investigate encoding of temporal information. Modulation transfer functions of responses were calculated in two ways: based on discharge rates (rMTFs) and on synchronization to the envelope (tMTFs). Among the variety of rMTFs, two types were readily identifiable: flat and band-pass. The responses of neurons exhibiting these types of rMTF differed in several ways. Neurons with flat rMTFs typically had moderate rates of spontaneous activity, sustained responses to short tone bursts, and low-pass or band-pass tMTFs. Neurons with band-pass rMTFs typically had low spontaneous activity, onset responses to short tone bursts, and flat tMTFs. The vast majority synchronized strongly to the modulation envelope. The best modulation frequencies of neurons with band-pass rMTFs extended from 14 to 283 Hz. The presence of neurons with band-pass rMTFs in the VNLL suggests that this nucleus plays a role in converting the temporal code for modulation frequency used in lower structures into a rate-based code for use higher in the auditory pathway. The substantial number of neurons with more complex modulation transfer functions indicates that the VNLL has other functions.


2009 ◽  
Vol 101 (4) ◽  
pp. 2002-2016 ◽  
Author(s):  
H.-R. Geis ◽  
J. G. G. Borst

Changes in the temporal envelope are important defining features of natural acoustic signals. Many cells in the inferior colliculus (IC) respond preferentially to certain modulation frequencies, but how they accomplish this is not yet clear. We therefore made whole cell patch-clamp recordings in the IC of anesthetized mice while presenting sinusoidal amplitude-modulated (SAM) tones. The relation between the number of evoked spikes and modulation frequency was used to construct rate modulation transfer functions (rMTFs). We observed different types of rate tuning, including band-pass (16%), band-reject (13%), high-pass (6%), and low-pass (6%) tuning. In the high-pass rMTF neurons and some of the low-pass rMTF neurons, the tuning characteristics appeared to be already present in the inputs. In both band-pass and band-reject rMTF neurons, the nonlinear relation between membrane potential and spike probability ensured preferential spiking during only a small part of the modulation period. Band-pass rMTF neurons had rapidly rising excitatory postsynaptic potentials, allowing good phase-locking to brief tones and intermediate modulation frequencies. At low modulation frequencies, adaptation of their spike threshold contributed to the onset response. In contrast, band-reject rMTF neurons responded with small excitatory or inhibitory postsynaptic potentials to brief tones. In these cells, a power law could describe the supralinear relation between average membrane potential and spike rate. Differences in timing of synaptic input and presence or absence of spike adaptation therefore define band-pass and band-reject rate tuning to SAM tones in the mouse IC.


1995 ◽  
Vol 74 (3) ◽  
pp. 1222-1243 ◽  
Author(s):  
P. Mukherjee ◽  
E. Kaplan

1. We investigated the time domain transformation that thalamocortical relay cells of the cat lateral geniculate nucleus (LGN) perform on their retinal input, and used computational modeling to explore the biophysical properties that determine the dynamics of the LGN relay cells in vivo. 2. We recorded simultaneously the input (S potentials) and output (action potentials) of 50 cat LGN relay cells stimulated by drifting sinusoidal gratings of varying temporal frequency. The temporal modulation transfer functions (TMTFs) of the neurons were derived from these data. The burstiness of the LGN spike trains was also assessed using objective criteria. 3. We found that the form of the TMTF was quite variable among cells, ranging from low-pass to strongly band-pass. The optimal temporal frequency of band-pass neurons was between 2 and 8 Hz. In addition, the TMTF of some cells was nonstationary: their temporal tuning changed with time. 4. The temporal tuning of a cell was directly related to the degree of burstiness of its spike train. Tonically firing relay cells had low-pass TMTFs, whereas the most bursty neurons exhibited the most sharply band-pass transfer functions. This was also true for single cells that altered their temporal tuning: a shift to more band-pass tuning was associated with increased burstiness of the spike train, and vice versa. 5. We constructed a computer simulation of the LGN relay cell. The model was a simplified five-channel version of the thalamocortical neuron model of McCormick and Huguenard. It incorporated the quantitative kinetics of the Ca2+ T channel, as well as the Hodgkin-Huxley Na+ and K+ channels, as the only active membrane currents. To simulate the in vivo dynamics of the relay cell, the input to the model consisted of trains of synaptic potentials, recorded as S potentials in our physiological experiments. 6. When the resting membrane potential of the model neuron was relatively depolarized, the model's TMTF was low-pass, with no bursting evident in the simulated spike train. At hyperpolarized resting membrane potentials, however, the modeled TMTF was band-pass, with frequent burst discharges. Thus the biophysical model reproduced not only the range of dynamics seen in real LGN relay cells, but also the dependence of the overall dynamics on the burstiness of the spike train. However, neither of these phenomena could be simulated without the T channel. Thus the simulations demonstrated that the T-type Ca2+ channel was necessary and sufficient to explain the LGN dynamics observed in physiological experiments.(ABSTRACT TRUNCATED AT 400 WORDS)


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