Elsevier

Hearing Research

Volume 274, Issues 1–2, April 2011, Pages 142-151
Hearing Research

Location of cells giving phase-locked responses to pure tones in the primary auditory cortex

https://doi.org/10.1016/j.heares.2010.05.012Get rights and content

Abstract

Phase-locked responses to pure tones have previously been described in the primary auditory cortex (AI) of the guinea pig. They are interesting because they show that some cells may use a temporal code for representing sounds of 60–300 Hz rather than the rate or place mechanisms used over most of AI. Our previous study had shown that the phase-locked responses were grouped together, but it was not clear whether they were in separate minicolumns or a larger macrocolumn. We now show that the phase-locked cells are arranged in a macrocolumn within AI that forms a subdivision of the isofrequency bands. Phase-locked responses were recorded from 158 multiunits using silicon based multiprobes with four shanks. The phase-locked units gave the strongest response in layers III/IV but phase-locked units were also recorded in layers II, V and VI. The column included cells with characteristic frequencies of 80 Hz–1.3 kHz (0.5–0.8 mm long) and was about 0.5 mm wide. It was located at a constant position at the intersection of the coronal plane 1 mm caudal to bregma and the suture that forms the lateral edge of the parietal bone.

Introduction

Most or all of the auditory cortex is thought to use a rate or place code for representing rhythmic fluctuations in a stimulus of more than about 100 Hz (Elhilali et al., 2004, Wang et al., 2008). However it is not surprising that a specialised group of auditory cells show phase-locking at up to 300 Hz because the potential information content of a timing code is much higher than a rate code (Tiesinga et al., 2008). It can also be more robust as firing rate is usually more sensitive to changes in sound intensity and neural habituation than time based codes. In the primary somatosensory cortex phase-locked responses, by single units, to the input derived from rapidly adapting receptors in the glabrous skin, are thought to be involved in the conscious discrimination of low-frequency (up to 80 Hz) vibrations (Mountcastle et al., 1969). Local field potential studies in the monkey and human auditory cortex have shown evidence of temporal synchronization to low-frequency tones and speech sounds (Steinschneider et al., 1980, Ahissar et al., 2001) and these responses may also be involved in conscious perception. Conscious perception may involve the synchronized activity of the neurons in at least one column of cells. Cylindrical or slab-like columns are thought to represent a basic processing unit in the neocortex (Mountcastle, 1997). A column is normally defined as a vertically arranged group of cells that stretches from layer I to layer VI where the cells have a consistent and definitive response property. In this study we wished to test three hypotheses: 1) that a phase-locked response to low-frequency tones (60–300 Hz) can be reliably found in every animal examined, 2) cells with phase-locked responses are arranged in a substantial group of cells that take the form of a column, 3) that the phase-locked responses are consistently located at a particular point on the cortical surface of the guinea pig.

In the auditory thalamus neurons are able to give phase-locked responses up to frequencies of over 1000 Hz (Rouiller et al., 1979, Wallace et al., 2007). Phase-locked responses to pure tones of up to 300 Hz have been described in AI of the guinea pig, but only for a small proportion of low-frequency cells and it was not clear whether the phase-locking lasted for more than 100 ms (Wallace et al., 2002). Some units showed strong habituation over a period of 100 ms. Stimuli of a longer duration were not tested in our earlier study.

Area AI in the cat was originally defined as a short-latency area with the majority of ascending inputs from the ventral nucleus of the medial geniculate body and a smooth tonotopic gradient among cells that had best frequencies of 100 Hz–40 kHz (Rose and Woolsey, 1949). However subsequent work has shown that AI can be subdivided with a functionally separate dorsal zone (Middlebrooks and Zook, 1983, He and Hashikawa, 1998). In some species there appear to be subdivisions along the tonotopic axis as well. Some rodents such as the mouse have a separate ultrasonic area which forms a continuation of the tonotopic gradient of AI (Stiebler et al., 1997). In other species with good low-frequency hearing the low-frequency end of AI (≤1.3 kHz) may also form a separate division that is particularly sensitive to timing information. We denote this as AI(LF). This division has many units that are sensitive to interaural phase differences (Fitzpatrick et al., 2000, Scott et al., 2009, Wallace and Palmer, 2009) and analyzing the time differences that these represent is an important element of localizing sounds in the azimuthal plane. We define AI(LF) as being the part of AI that contains cells that are sensitive to interaural timing differences. In the guinea pig inferior colliculus timing-sensitive neurons generally have a CF of ≤1.5 kHz (McAlpine et al., 1996) and a slightly lower cut-off point (1.3 kHz) is present in the cortex (Wallace and Palmer, 2009). Coding for interaural time differences requires a reasonable population of cells with CFs that are less than 1 kHz. Small rodents such as the mouse, with relatively poor low-frequency hearing, may not have a separate AI(LF) (Stiebler et al., 1997). We have previously shown that phase-locked responses to pure tones form about 13% of units in AI(LF) in the guinea pig (Wallace et al., 2002). In this study by using multi-electrodes to give simultaneous recordings, at fixed intervals across the length and depth of the cortex, we were able to sample a greater number of units than in our previous single electrode work.

Section snippets

Surgical preparation

Eight pigmented, adult guinea pigs of both sexes and weighing 322–702 g were used for physiological recording. Animals were anaesthetized with urethane (0.9 g/kg i.p., in 20% solution in 0.9% saline) supplemented as necessary by 0.1 ml Hypnorm (fentanyl citrate 0.315 mg/ml; fluanisone 10 mg/ml i.m.) to maintain forepaw areflexia. A single dose of atropine sulphate (0.06 mg/kg s.c.) was given to reduce bronchial secretions. All animals were tracheotomised and core temperature was maintained at

Characteristics of phase-locked responses

We made a total of 26 placements of the four-pronged recording array in the AI(LF) of eight animals and identified phase-locked responses to tones in the range of 60–350 Hz for a total of 158 multiunits. The strength of phase-locking, as measured by the vector strength, varied between units and also varied between frequencies for any one multiunit. The most effective frequency for producing a phase-locked response varied between 60 and 140 Hz and the vector strengths varied between 0.08 and

Columnar arrangement of phase-locked responses

The results of this study are consistent with the suggestion that all guinea pigs have neurons at the low-frequency end of AI that can show phase-locked responses to tone pips in the range of 60–320 Hz. In each of the eight experiments where we systematically searched for phase-locked responses we found a discrete column of cells that gave phase-locked responses over these frequencies. In our previous studies of phase-locked responses in AI (Wallace et al., 2002) and in the ventrorostral belt (

Acknowledgements

Silicon probes were generously provided by the University of Michigan Center for Neural Communication Technology sponsored by NIH/NCRR grant P41 RR09754. We want to thank O Zobay for statistical help and Dr JWH Schnupp for sending us a copy of Brainware.

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