Intracellular Recordings From Combination-Sensitive Neurons in the Inferior Colliculus

Abstract

Peterson DC, Voytenko S, Gans D, Galazyuk A, Wenstrup J. Intracellular recordings from combination-sensitive neurons in the inferior colliculus. J Neurophysiol 100: 629-645, 2008. First published May 21, 2008 doi:10.1152/jn.90390.2008. In vertebrate auditory systems, specialized combination-sensitive neurons analyze complex vocal signals by integrating information across multiple frequency bands. We studied combinationsensitive interactions in neurons of the inferior colliculus (IC) of awake mustached bats, using intracellular somatic recording with sharp electrodes. Facilitated combinatorial neurons are coincidence detectors, showing maximum facilitation when excitation from low-and high-frequency stimuli coincide. Previous work showed that facilitatory interactions originate in the IC, require both low and high frequency-tuned glycinergic inputs, and are independent of glutamatergic inputs. These results suggest that glycinergic inputs evoke facilitation through either postinhibitory rebound or direct depolarizing mechanisms. However, in 35 of 36 facilitated neurons, we observed no evidence of low frequency-evoked transient hyperpolarization or depolarization that was closely related to response facilitation. Furthermore, we observed no evidence of shunting inhibition that might conceal inhibitory inputs. Since these facilitatory interactions originate in IC neurons, the results suggest that inputs underlying facilitation are electrically segregated from the soma. We also recorded inhibitory combinatorial interactions, in which low frequency sounds suppress responses to higher frequency signals. In 43% of 118 neurons, we observed low frequency-evoked hyperpolarizations associated with combinatorial inhibition. For these neurons, we conclude that low frequency-tuned inhibitory inputs terminate on neurons primarily excited by high-frequency signals; these inhibitory inputs may create or enhance inhibitory combinatorial interactions. In the remainder of inhibited combinatorial neurons (57%), we observed no evidence of low frequency-evoked hyperpolarizations, consistent with observations that inhibitory combinatorial responses may originate in lateral lemniscal nuclei.

Properties of echo delay-tuning receptive fields in the inferior colliculus of the mustached bat

“…Neurons were considered to be combination-sensitive if, with pairs of PT and/or FM pulses stimulation, their spike discharge to combination stimuli was !20% higher (for facilitation) or !20% lower for suppression than the sum of their spikes in response to separate single high and low-frequency tone-burst stimuli (Peterson et al, 2008). Combination-sensitive responses showed either facilitated or suppressed responses.…”

“…while the cortical experiments typically emphasized responses to sonar elements Wenstrup, 1999, 2004;Wenstrup and Portfors, 2011;Suga and O'Neill, 1979;O'Neill and Suga, 1979;Suga et al, 1983;O'Neill, 1995). In intracellular recording experiments, Peterson et al (2008) suggested that the distribution and types of combination-sensitive interactions in the IC neuronal population are not dependent on tonal or FM stimulation. However, both types of stimulation have not been tested in the same neuron.…”

Differential roles of GABAergic and glycinergic input on FM selectivity in the inferior colliculus of the pallid bat

“…Other examples of the latter are the creation of delay tuning in the mustached bat IC, which is shaped by a combination of inherited selectivity and selectivity shaped at the level of the IC (Peterson et al 2008) and the transformation of binaural response properties in the auditory brain stem (Pollak et al 2002). Fig.…”

“…1995). However, there are known to be considerable species differences (e.g., Peterson et al 2008) in the functional neuroanatomy of the lateral lemniscal nuclei, making such speculation problematic. Fig.…”

Phoneme and word recognition in the auditory ventral stream

“…In the case of speech sounds, these neurons conjoin representations for adjacent speech formants or, at higher levels, adjacent phonemes. Although the mechanism by which combination sensitivity (CS) is directionally selective in the temporal domain is not fully understood, some propositions exist (22)(23)(24)(25)(26). As an empirical matter, direction selectivity is clearly present early in auditory cortex (19,27).…”