Ian A. Harrington

Location coding by opponent neural populations in the auditory cortex.

Although the auditory cortex plays a necessary role in sound localization, physiological investigations in the cortex reveal inhomogeneous sampling of auditory space that is difficult to reconcile with localization behavior under the assumption of local spatial coding. Most neurons respond maximally to sounds located far to the left or right side, with few neurons tuned to the frontal midline. Paradoxically, psychophysical studies show optimal spatial acuity across the frontal midline. In this paper, we revisit the problem of inhomogeneous spatial sampling in three fields of cat auditory cortex. In each field, we confirm that neural responses tend to be greatest for lateral positions, but show the greatest modulation for near-midline source locations. Moreover, identification of source locations based on cortical responses shows sharp discrimination of left from right but relatively inaccurate discrimination of locations within each half of space. Motivated by these findings, we explore an opponent-process theory in which sound-source locations are represented by differences in the activity of two broadly tuned channels formed by contra- and ipsilaterally preferring neurons. Finally, we demonstrate a simple model, based on spike-count differences across cortical populations, that provides bias-free, level-invariant localization—and thus also a solution to the “binding problem” of associating spatial information with other nonspatial attributes of sounds.

Tinnitus in hamsters following exposure to intense sound

Hamsters were trained with a conditioned suppression/avoidance procedure to drink in the presence of a broadband noise and/or a tone and to stop drinking in the absence of sound. A variety of tones and loudspeaker locations were used during training so that the animals would respond to a sound regardless of its frequency or location. Four groups of animals then had their left ears exposed to a 10-kHz tone at 124 or 127 dB for 0.5, 1, 2 or 4 h. They were then tested for tinnitus by comparing their performance with that of unexposed animals to determine if they behaved as if they perceived a sound when no external sound was present. The groups exposed for 2 and 4 h tested positive for tinnitus whereas those exposed for 0.5 and 1 h did not. The degree of hearing loss produced by the tone exposure was assessed using behavioral and auditory brainstem response (ABR) procedures. A partial dissociation was found between the hearing loss, as estimated by the ABR, and the results of the tinnitus test in that animals exposed for 1 h had the same hearing loss as the 2- and 4-h exposed animals, but did not test positive for tinnitus. This suggests that the positive scores on the tinnitus test were not due to hearing loss. These results are discussed along with those of previous behavioral studies of tinnitus in animals.

Spatial sensitivity of neurons in the anterior, posterior, and primary fields of cat auditory cortex.

We assessed the spatial-tuning properties of units in the cats anterior auditory field (AAF) and compared them with those observed previously in the primary (A1) and posterior auditory fields (PAF). Multi-channel, silicon-substrate probes were used to record single- and multi-unit activity from the right hemispheres of alpha-chloralose-anesthetized cats. Spatial tuning was assessed using broadband noise bursts that varied in azimuth or elevation. Response latencies were slightly, though significantly, shorter in AAF than A1, and considerably shorter in both of those fields than in PAF. Compared to PAF, spike counts and latencies were more poorly modulated by changes in stimulus location in AAF and A1, particularly at higher sound pressure levels. Moreover, units in AAF and A1 demonstrated poorer level tolerance than units in PAF with spike rates modulated as much by changes in stimulus intensity as changes in stimulus location. Finally, spike-pattern-recognition analyses indicated that units in AAF transmitted less spatial information, on average, than did units in PAF-an observation consistent with recent evidence that PAF is necessary for sound-localization behavior, whereas AAF is not.

“Central” auditory gap detection: A spatial case

Normal listeners were tested for their temporal auditory gap detection thresholds using free-field presentation of white-noise stimuli delivered from the left (L) and right (R) poles of the interaural axis. The noise bursts serving as the leading and trailing markers for the silent period were presented in either the same (LL,RR) or different (LR,RL) auditory locations. The duration of the leading marker was a second independent variable. Gap thresholds for stimuli in which the markers had the same location were low, and usually were independent of the duration of the leading marker. Gap thresholds for the LR and RL conditions were longer. These gap thresholds were sensitive to the duration of the leading marker, and increased as the leading marker duration decreased. This finding is consistent with the hypothesis that a relative timing operation mediates gap detection when the markers activate different perceptual channels. The present data suggest that this timing process can operate on perceptual channels emerging from central nervous system processing.

An investigation of sensory deficits underlying the aphasia-like behavior of macaques with auditory cortex lesions.

Bilateral auditory cortex lesions in Japanese macaques result in an aphasia-like deficit in which the animals are unable to discriminate two forms of their coo vocalizations. To determine whether this deficit is sensory in nature, two monkeys with bilateral lesions were tested for their ability to discriminate frequency and frequency change. The results indicated that although the animals were able to discriminate between sounds of different frequencies, they were unable to determine whether a sound was changing in frequency. Because the animals’ coo vocalizations differ primarily in the predominant direction of their frequency change and not in their absolute frequency content, the aphasia-like deficit of animals with bilateral auditory cortex lesions appears to be a sensory disorder.

Sound Localization and the Auditory Cortex

This chapter reviews the representation of sound-source locations in the auditory cortex. It begins with a description of the spatial sensitivity of single neurons, beginning with the primary auditory cortex (A1) in cats and ferrets, and then reviewing recent surveys of the second auditory area (A2), the anterior ectosylvian sulcus area, the anterior auditory field, the posterior auditory field, and the dorsal zone of A1. Topics include spatial receptive fields, spatial topography, spatial sensitivity in anesthetized-versus-unanesthetized conditions, responses to dynamic sounds and multiple sound sources, derivation of spatial sensitivity from acoustic cues, and responses in nonhuman primates. Next, the problem is addressed as to how an animal, or an investigator, might identify the location of a sound source strictly on the basis of patterns of cortical activity. The effects of cortical inactivation on sound-localization behavior are reviewed, including studies using classical lesion techniques as well as newer reversible inactivation techniques. Finally, the role of the human auditory cortex in sound localization is addressed in the context of the clinical lesion literature supplemented by modern structural imaging techniques and in the context of the rapidly emerging use of functional imaging.