Information Processing by Onset Neurons in the Cat Auditory Brainstem

Abstract

Octopus cells in the ventral cochlear nucleus (VCN) have been difficult to study because of the very features that distinguish them from other VCN neurons. We performed in vivo recordings in cats on well-isolated units, some of which were intracellularly labeled and histologically reconstructed. We found that responses to low-frequency tones with frequencies G 1 kHz reveal higher levels of neural synchrony and entrainment to the stimulus than the auditory nerve. In responses to higher frequency tones, the neural discharges occur mostly near the stimulus onset. These neurons also respond in a unique way to 100 % amplitude-modulated (AM) tones with discharges exhibiting a bandpass tuning. Responses to frequency-modulated sounds (FM) are unusual: Octopus cells react more vigorously during the ascending than the descending parts of the FM stimulus. We examined responses of neurons in the ventral nucleus of the lateral lemniscus (VNLL) whose discharges to tones and AM sounds are similar to octopus cells. Repeated stimulation with short tone pips of VCN and VNLL onset neurons evokes trains of action potentials with gradual shifts toward later times in their first spike latency. This behavior parallels short-term post-synaptic depression observed by other authors in in vitro VCN recordings of octopus cells. VCN and VNLL onset units in cats respond to frozen noise stimuli with gaps as narrow as 1 ms with a robust discharge near the stimulus onset following the gap. This finding suggests that VCN and VNLL onset cells play a role in gap detection, which is of great importance to speech perception.

Mammalian octopus cells are direction selective to frequency sweeps by synaptic sequence detection

“…Figure 5D shows responses to pure and AM tones at 70 dB SPL. Consistent with previous reports (Recio-Spinoso and Rhode, 2020;Rhode, 1994), AM stimuli evoke much higher sustained spike responses than pure tones. Remarkably, the responses area to AM tones reveals three discontinuous regions, and the carrier frequencies triggering the responses largely match the triggering frequencies in responses to Schroeder stimuli.…”

“…With the cochlea being mapped in frequency, the closest equivalent to motion on the retina or skin is "cochlear motion" caused by changes in sound frequency. Use of various forms of FM has uncovered direction selectivity at multiple anatomical levels, including the cochlear nucleus of diverse species [bat (Suga, 1964), guinea pig (Paraouty et al, 2018), rat (Møller, 1974), and cat (Britt and Starr, 1976;Erulkar et al, 1968;Godfrey et al, 1975;Møller, 1974;Recio-Spinoso and Rhode, 2020;Rhode and Smith, 1986)]. The speeds tested were several orders of magnitude slower than those used here (>1 kHz/ms), and revealed modest direction selectivity in the small number of presumed octopus cells sampled, mostly favoring upward sweeps (Godfrey et al, 1975;Paraouty et al, 2018;Recio-Spinoso and Rhode, 2020;Rhode and Smith, 1986).…”

“…Use of various forms of FM has uncovered direction selectivity at multiple anatomical levels, including the cochlear nucleus of diverse species [bat (Suga, 1964), guinea pig (Paraouty et al, 2018), rat (Møller, 1974), and cat (Britt and Starr, 1976; Erulkar et al, 1968; Godfrey et al, 1975; Møller, 1974; Recio-Spinoso and Rhode, 2020; Rhode and Smith, 1986)]. The speeds tested were several orders of magnitude slower than those used here (>1 kHz/ms), and revealed modest direction selectivity in the small number of presumed octopus cells sampled, mostly favoring upward sweeps (Godfrey et al, 1975; Paraouty et al, 2018; Recio-Spinoso and Rhode, 2020; Rhode and Smith, 1986). One study in chinchilla found “little additional processing” in cochlear nucleus responses to Schroeder stimuli but did not report responses from octopus cells (Recio, 2001).…”

“…Long, 300-600 ms tones were delivered at various carrier frequencies, mostly ranging from 0.5 -40 kHz in 0.4 octave steps. Because sinusoidally amplitude modulated (AM) tones are a more effective stimulus to drive octopus cells, often at lower threshold, than pure tones (Recio-Spinoso and Rhode, 2020;Rhode, 1994), while still being narrowband, we sometimes resorted to the use of these long AM tones (modulation depth 100%, modulation frequency of 100 Hz, rise/fall time 5 ms) to study the frequency tuning of the cell and obtain a BF. The AM tones were generated according to:…”

Minimal Number of Required Inputs for Temporally Precise Action Potential Generation in Auditory Brainstem Nuclei

“…VNLL neurons phase lock to the sound onset and follow modulation frequencies of 10-300 Hz ideal for coding envelope sound structures (Zhang and Kelly, 2006;Recio-Spinoso and Joris, 2014) to generate rapid onset inhibition in the inferior colliculus (Pollak et al, 2011;Moore and Trussell, 2017). The more transient responsiveness of VNLL neurons may be helpful to cost-effectively relay their octopus cell inputs, known to transmit broadband sound onsets (Smith et al, 2005;Recio-Spinoso and Rhode, 2020), to the inferior colliculus. MNTB neurons phase lock to stimulations of more than 500 Hz with low failure rates (Guinan and Li, 1990;Lorteije et al, 2009).…”