The Neurophysiology of Pitch

Abstract

The representation of the pitch of a sound would appear to be a simple affair; the cochlea performs a spectral analysis of incoming sound and maps stimulus frequency onto place along the basilar membrane (BM). These mapped frequencies are then signaled to the brain via the auditory nerve (see Robles and Ruggero 2001 for a review). This tonotopic representation of a sound is often simulated using a computational model in which the membrane motion is represented by a bank of “auditory” filters (e.g., Patterson et al. 1995). The output of each filter is half-wave rectified and integrated to determine the activity level in that filter, and the set of levels is then plotted as a function of filter centre frequency (or cochlear place) to produce what is referred to as an “auditory spectrum” (see Fig. 2.3 in Plack and Oxenham, Chapter 2). This representation of tonotopic activity is often assumed to be the basis of pitch perception (e.g., Cohen et al. 1995). It is also the case, however, that the inner hair cells (IHCs) transduce movement of the basilar membrane in-phase up to relatively high frequencies (e.g., approximately 5 kHz in the cat [Felis catus, Johnson 1980]; 3.5 kHz in the guinea pig [Cavia porcellus, Palmer and Russell 1986]). As a result, there is information about the timing of membrane peaks in each tonotopic channel. To make use of this information models have been developed that subject each frequency channel to autocorrelation (Slaney and Lyon 1990; Meddis and Hewitt 1991a), or some other form of temporal analysis (e.g., strobed temporal integration [Patterson et al. 1995]). The resulting two-dimensional representation (filter-center-frequency versus delay or time-interval) exhibits activity peaks across a range of channels at the period of pitch-producing sounds. Proponents of temporal models argue that it is this distribution of activity in these “auto- correlograms” that determines the perceived pitch (e.g., Meddis and Hewitt 1991a,b; Yost et al. 1996). In this context this chapter reviews the evidence that pitch is encoded by place, timing, or a combination of the two by examining the correspondences between neural patterns of activity at various stages along the auditory pathway, and the auditory percept of pitch. Strictly speaking, all the studies that are discussed in this chapter will be searching for a neural representation of the pitch of simple and complex sounds; much of the work has taken place using anesthetized preparations and thus one is forced to look only for representations and not a code. The concept of a neural code is reserved for the set of rules that relates behavior to neural activity (Eggermont 2001). Of necessity the neural activity has been recorded from nonhuman animals and this places an important constraint on the interpretation of any neural representation of pitch. The problems and successes of using animals to study the perception of pitch are discussed in detail by Shofner (Chapter 3). This chapter reflects the amount of information we have for the various parts of the auditory pathway; this information becomes increasingly sparse as we ascend from the auditory nerve to the auditory cortex. Although we arguably have most information about the mammalian cochlea, this chapter does not review the cochlea in any significant detail. For this information the interested reader is referred to reviews that can be found in a companion volume in the Springer Handbook of Auditory Research, Volume 8, The Cochlea. For a review of models of the processing of pure tones the reader is referred to the review by Delgutte (1996) (Springer Handbook of Auditory Research, Vol. 6: Auditory Computation). A review of models of the pitch of simple and complex sounds is provided by de Cheveigne (Chapter 6).