Temporal and Spectral Sensitivity of Complex Auditory Neurons in the Nucleus HVc of Male Zebra Finches

Abstract

Complex vocalizations, such as human speech and birdsong, are characterized by their elaborate spectral and temporal structure. Because auditory neurons of the zebra finch forebrain nucleus HVc respond extremely selectively to a particular complex sound, the bird's own song (BOS), we analyzed the spectral and temporal requirements of these neurons by measuring their responses to systematically degraded versions of the BOS. These synthetic songs were based exclusively on the set of amplitude envelopes obtained from a decomposition of the original sound into frequency bands and preserved the acoustical structure present in the original song with varying degrees of spectral versus temporal resolution, which depended on the width of the frequency bands. Although both excessive temporal or spectral degradation eliminated responses, HVc neurons responded well to degraded synthetic songs with timefrequency resolutions of ϳ5 msec or 200 Hz. By comparing this neuronal time-frequency tuning with the time-frequency scales that best represented the acoustical structure in zebra finch song, we concluded that HVc neurons are more sensitive to temporal than to spectral cues. Furthermore, neuronal responses to synthetic songs were indistinguishable from those to the original BOS only when the amplitude envelopes of these songs were represented with 98% accuracy. That level of precision was equivalent to preserving the relative time-varying phase across frequency bands with resolutions finer than 2 msec. Spectral and temporal information are well known to be extracted by the peripheral auditory system, but this study demonstrates how precisely these cues must be preserved for the full response of high-level auditory neurons sensitive to learned vocalizations.

Intrinsic and Extrinsic Contributions to Auditory Selectivity in a Song Nucleus Critical for Vocal Plasticity

“…To quantif y each neuron's response strength, the psychophysical measure dЈ (Green and Swets, 1966), which represents the discriminability between two stimuli, was used to compare BOS with reversed-BOS responses. A difference in response to these two stimuli has been used previously as the criterion for selectivity of neurons in L M AN, as well as in H Vc (Solis and Doupe, 1997;Theunissen and Doupe, 1998). The dЈ value for the discriminability of the response to BOS versus that to reversed BOS was calculated as:…”

Mechanisms of Temporal Auditory Pattern Recognition in Songbirds

“…Farther along the ascending sensory hierarchy, the caudal-medial nidopallium (NCM) and the lateral and medial regions of the caudal mesopallium (CLM, CMM) are analogous to mammalian secondary auditory cortices. Neurons throughout the starling auditory forebrain show complex patterns of tonotopic organization (Capsius & Leppelsack, 1996;Haüsler, 1996;Leppelsack & Schwartzkopff, 1972;Rübsamen & Dörrscheidt, 1986), including selectivity to species-specific vocalizations (Bonke, Bonke, & Scheich, 1979;Leppelsack & Vogt, 1976;Müller & 162 GENTNER Leppelsack, 1985;Theunissen & Doupe, 1998;Theunissen & Shaevitz, 2006). In other songbirds, the general pattern of increasing response selectivity along the sensory hierarchy (Hsu, Woolley, Fremouw, & Theunissen, 2004;Woolley, Fremouw, Hsu, & Theunissen, 2005) continues into NCM and CMM/CLM (Sen, Theunissen, & Doupe, 2001), suggesting that these regions are involved in the extraction of complex features (Chew, Mello, Nottebohm, Jarvis, & Vicario, 1995;Chew, Vicario, & Nottebohm, 1996;Grace, Amin, Singh, & Theunissen, 2003;Leppelsack, 1983;Sen et al, 2001;Stripling, Volman, & Clayton, 1997).…”

Neural coding of naturalistic motion stimuli

“…To meet the challenge we must modify both our experimental designs and our methods for analyzing the responses to these much more complicated inputs. Recent examples of laboratory based approaches to the problem of natural stimulation are studies of bullfrog auditory neurons responding to synthesized frog calls (Rieke et al , 1995), insect olfactory neurons responding to odour plumes (Vickers et al , 2001), cat LGN cells responding to movies (Dan et al , 1996, Stanley et al , 1999, primate visual cortical cells during free viewing of natural images (Gallant et al , 1998, Vinje andGallant, 2000), auditory neurons in song birds stimulated by song and song-like signals (Theunissen and Doupe, 1998, Theunissen et al , 2000, the responses in cat auditory cortex to signals with naturalistic statistical properties (Rotman et al , 1999), and motion sensitive cells in the fly Egelhaaf, 2001, de Ruyter van Steveninck et al , 2001). In each case compromises are struck between well controlled stimuli with understandable statistical properties and the fully natural case.…”