Computational Diversity in the Cochlear Nucleus Angularis of the Barn Owl

Abstract

The cochlear nucleus angularis (NA) is widely assumed to form the starting point of a brain stem pathway for processing sound intensity in birds. Details of its function are unclear, however, and its evolutionary origin and relationship to the mammalian cochlear-nucleus complex are obscure. We have carried out extracellular single-unit recordings in the NA of ketamine-anesthetized barn owls. The aim was to re-evaluate the extent of heterogeneity in NA physiology because recent studies of cellular morphology had established several distinct types. Extensive characterization, using tuning curves, phase locking, peristimulus time histograms and rate-level functions for pure tones and noise, revealed five major response types. The most common one was a primary-like pattern that was distinguished from auditory-nerve fibers by showing lower vector strengths of phase locking and/or lower spontaneous rates. Two types of chopper responses were found (chopper-transient and a rare chopper-sustained), as well as onset units. Finally, we routinely encountered a complex response type with a pronounced inhibitory component, similar to the mammalian typeIV. Evidence is presented that this range of response types is representative for birds and that earlier conflicting reports may be due to methodological differences. All five response types defined were similar to well-known types in the mammalian cochlear nucleus. This suggests convergent evolution of neurons specialized for encoding different behaviorally relevant features of the auditory stimulus. It remains to be investigated whether the different response types correlate with morphological types and whether they establish different processing streams in the auditory brain stem of birds.

Difference in Response Reliability Predicted by Spectrotemporal Tuning in the Cochlear Nuclei of Barn Owls

“…NA and NM units had significantly different response latencies (NA: 1.9 ± 0.51 ms; NM: 2.25 ± 0.34 ms; medians significantly different by Kruskal-Wallis, p<0.005). Compared to response latencies previously reported for NM and NA (Sullivan and Konishi, 1984; Köppl and Carr, 2003, respectively), our values are about 0.5 ms shorter. However, both previous studies used PSTHs of responses to tone and/or noise stimuli with onset ramps to estimate first-spike latency.…”

“…We observed a mean response rate of 183 ± 110 spikes/s in our sample of primary-like NA units, measured during the first 50 ms of their response to unfrozen noise. This value is lower than that reported by Köppl and Carr (2003). Theirs, however, is saturation rate measured with tone stimulation, which makes the difference difficult to interpret.…”

Difference in Response Reliability Predicted by Spectrotemporal Tuning in the Cochlear Nuclei of Barn Owls

“…NA and NM units had significantly different response latencies (NA: 1.9 ± 0.51 ms; NM: 2.25 ± 0.34 ms; medians significantly different by Kruskal-Wallis, p<0.005). Compared to response latencies previously reported for NM and NA (Sullivan and Konishi, 1984; Köppl and Carr, 2003, respectively), our values are about 0.5 ms shorter. However, both previous studies used PSTHs of responses to tone and/or noise stimuli with onset ramps to estimate first-spike latency.…”

“…We observed a mean response rate of 183 ± 110 spikes/s in our sample of primary-like NA units, measured during the first 50 ms of their response to unfrozen noise. This value is lower than that reported by Köppl and Carr (2003). Theirs, however, is saturation rate measured with tone stimulation, which makes the difference difficult to interpret.…”

Tonotopic organization of the superior olivary nucleus in the chicken auditory brainstem

“…Complexity and diversity of SON neuronal responses may derive from their multiple inputs. SON responses resemble the varied response types observed in NA neurons (Sachs et al, 1978; Carr and Soares, 2002; Koppl and Carr, 2003). Additionally, sustained responses in SON may also be evoked by sustained NL neuron inputs, which are weakly driven by monaural stimulation (Pena et al, 1996).…”

Response Properties of Single Neurons in the Zebra Finch Auditory Midbrain: Response Patterns, Frequency Coding, Intensity Coding, and Spike Latencies

“…Of the cells showing ongoing responses, 3 distinct temporal response patterns were observed. These 3 response patterns correspond to the "primary-like," "sustained," and "primarylike with notch" response patterns observed in single neurons of both mammalian and avian auditory nuclei (Koppl and Carr 2003;Pollak et al 1978;Syka et al 2000;Warchol and Dallos 1990). All consistent responses fell into 4 categories: 1) onset, in which a few spikes were locked to the onset of the stimulus;…”

Difference in Response Reliability Predicted by Spectrotemporal Tuning in the Cochlear Nuclei of Barn Owls

“…NA and NM units had significantly different response latencies (NA: 1.9 ± 0.51 ms; NM: 2.25 ± 0.34 ms; medians significantly different by Kruskal-Wallis, p<0.005). Compared to response latencies previously reported for NM and NA (Sullivan and Konishi, 1984; Köppl and Carr, 2003, respectively), our values are about 0.5 ms shorter. However, both previous studies used PSTHs of responses to tone and/or noise stimuli with onset ramps to estimate first-spike latency.…”

“…We observed a mean response rate of 183 ± 110 spikes/s in our sample of primary-like NA units, measured during the first 50 ms of their response to unfrozen noise. This value is lower than that reported by Köppl and Carr (2003). Theirs, however, is saturation rate measured with tone stimulation, which makes the difference difficult to interpret.…”

Tonotopic organization of the superior olivary nucleus in the chicken auditory brainstem

“…Complexity and diversity of SON neuronal responses may derive from their multiple inputs. SON responses resemble the varied response types observed in NA neurons (Sachs et al, 1978; Carr and Soares, 2002; Koppl and Carr, 2003). Additionally, sustained responses in SON may also be evoked by sustained NL neuron inputs, which are weakly driven by monaural stimulation (Pena et al, 1996).…”

Response Properties of Single Neurons in the Zebra Finch Auditory Midbrain: Response Patterns, Frequency Coding, Intensity Coding, and Spike Latencies

“…Of the cells showing ongoing responses, 3 distinct temporal response patterns were observed. These 3 response patterns correspond to the "primary-like," "sustained," and "primarylike with notch" response patterns observed in single neurons of both mammalian and avian auditory nuclei (Koppl and Carr 2003;Pollak et al 1978;Syka et al 2000;Warchol and Dallos 1990). All consistent responses fell into 4 categories: 1) onset, in which a few spikes were locked to the onset of the stimulus;…”

Difference in Response Reliability Predicted by Spectrotemporal Tuning in the Cochlear Nuclei of Barn Owls

“…NA and NM units had significantly different response latencies (NA: 1.9 ± 0.51 ms; NM: 2.25 ± 0.34 ms; medians significantly different by Kruskal-Wallis, p<0.005). Compared to response latencies previously reported for NM and NA (Sullivan and Konishi, 1984; Köppl and Carr, 2003, respectively), our values are about 0.5 ms shorter. However, both previous studies used PSTHs of responses to tone and/or noise stimuli with onset ramps to estimate first-spike latency.…”

“…We observed a mean response rate of 183 ± 110 spikes/s in our sample of primary-like NA units, measured during the first 50 ms of their response to unfrozen noise. This value is lower than that reported by Köppl and Carr (2003). Theirs, however, is saturation rate measured with tone stimulation, which makes the difference difficult to interpret.…”

Tonotopic organization of the superior olivary nucleus in the chicken auditory brainstem

“…Complexity and diversity of SON neuronal responses may derive from their multiple inputs. SON responses resemble the varied response types observed in NA neurons (Sachs et al, 1978; Carr and Soares, 2002; Koppl and Carr, 2003). Additionally, sustained responses in SON may also be evoked by sustained NL neuron inputs, which are weakly driven by monaural stimulation (Pena et al, 1996).…”

Response Properties of Single Neurons in the Zebra Finch Auditory Midbrain: Response Patterns, Frequency Coding, Intensity Coding, and Spike Latencies

“…Of the cells showing ongoing responses, 3 distinct temporal response patterns were observed. These 3 response patterns correspond to the "primary-like," "sustained," and "primarylike with notch" response patterns observed in single neurons of both mammalian and avian auditory nuclei (Koppl and Carr 2003;Pollak et al 1978;Syka et al 2000;Warchol and Dallos 1990). All consistent responses fell into 4 categories: 1) onset, in which a few spikes were locked to the onset of the stimulus;…”