Encoding timing and intensity in the ventral cochlear nucleus of the cat

Abstract

Physiological response properties of neurons in the ventral cochlear nucleus have a variety of features that are substantially different from the stereotypical auditory nerve responses that serve as the principal source of activation for these neurons. These emergent features are the result of the varying distribution of auditory nerve inputs on the soma and dendrites of the various cell types within the nucleus; the intrinsic membrane characteristics of the various cell types causing different responses to the same input in different cell types; and secondary excitatory and inhibitory inputs to different cell types. Well-isolated units were recorded with high-impedance glass microelectrodes, both intracellularly and extracellularly. Units were characterized by their temporal response to short tones, rate vs. intensity relation, and response areas. The principal response patterns were onset, chopper, and primary-like. Onset units are characterized by a well-timed first spike in response to tones at the characteristic frequency. For frequencies less than 1 kHz, onset units can entrain to the stimulus frequency with greater precision than their auditory nerve inputs. This implies that onset units receive converging inputs from a number of auditory nerve fibers. Onset units are divided into three subcategories, OC, OL, and OI. OC units have extraordinarily wide dynamic ranges and low-frequency selectivity. Some are capable of sustaining firing rates of 800 spikes/s at high intensities. They have the smallest standard deviation and coefficient of variation of the first spike latency of any cells in the cochlear nuclei. OC units are candidates for encoding intensity. OI and OL units differ from OC units in that they have dynamic ranges and frequency selectivity ranges much like those of auditory nerve fibers. They differ from one another in their steady-state firing rates; OI units fire mainly at the onset of a tone. OI units also differ from OL units in that they prefer frequency sweeps in the low to high direction. Primary-like-with-notch (PLN) units also respond to tones with a well-timed first spike. They differ from onset cells in that the onset peak is not always as precise as the spontaneous rate is higher. A comparison of spontaneous firing rate and saturation firing rate of PLN units with auditory nerve fibers suggest that PLN units receive one to four auditory nerve fiber inputs. Chopper units fire in a sustained regular manner when they are excited by sound.(ABSTRACT TRUNCATED AT 400 WORDS)

A Functional Point-Neuron Model Simulating Cochlear Nucleus Ideal Onset Responses

“…The synchronization coefficient, calculated from the model PSTH, is 0.99. This is in good agreement with recorded synchronization coefficients of O I units (Rhode and Smith, 1986).…”

“…Godfrey et al (1975) found that O I unit responses to pure-tone stimuli ( f > 2 kHz) reveal one sharply timed action potential at stimulus onset followed by no or little (<10 spikes/s) subsequent activity during the sustained portion of the tone. He concluded that these ideal onset responses that were confirmed in a number of subsequent studies (e.g., Rhode and Smith, 1986;Rhode, 1994) can be associated with octopus cell responses. In contrast to their onset response at high stimulus frequencies, O I units can entrain to low-frequency pure tones ( f < 800 Hz), where they emit exactly one spike at each stimulus cycle (e.g., Rhode and Smith, 1986), if the stimulus frequency is included in the cell's frequency-response area.…”

“…In contrast to their onset response at high stimulus frequencies, O I units can entrain to low-frequency pure tones ( f < 800 Hz), where they emit exactly one spike at each stimulus cycle (e.g., Rhode and Smith, 1986), if the stimulus frequency is included in the cell's frequency-response area. The synchronization coefficient of low-frequency pure-tone entrainment lies between 0.9 and 0.99 (Rhode and Smith, 1986), indicating a nearly perfect synchronization of the cell's response to the stimulus frequency.…”

“…The upper left panel of Fig. 4 shows a recorded frequency-response area of an O I unit (CF = 2.2 kHz), replotted from Rhode and Smith (1986). The CF puretone threshold was at 30 dB SPL, and the stimulus level was increased in 10-dB steps from 10 to 60 dB with respect to the unit's pure-tone threshold (reThr).…”

“…Thus, onset units of the ventral cochlear nucleus (VCN) are commonly divided into three groups, based on their peri-stimulus time histograms (PSTH) in response to high-frequency tone bursts: onset with late or long-lasting activity (O L ), onset with chopping (O C ), revealing two or more peaks that are not related to the stimulus frequency, and ideal onset (O I ) (Godfrey et al, 1975;Rhode and Smith, 1986;Winter and Palmer, 1995). Despite the ongoing stimulation provided by the AN fibers, O I units show one precisely timed action potential at the tone onset followed by no or little (<10 spikes/s) subsequent activity when stimulated at their characteristic frequency (CF) (e.g., Godfrey et al, 1975;Rhode and Smith, 1986). Another remarkable feature of O I units is their entrainment, i.e., the generation of exactly one spike per stimulus period, in response to low-frequency pure tones, click trains and amplitude modulated (AM) stimuli presented at repetition/modulation rates <800 Hz.…”