Introduction
Mammalian hearing is subserved by a complex and interconnected system of bilaterally-located nuclei. As illustrated in the schematic to the right, incoming information about the acoustic environment enters the brain via the auditory nerve (AN), whose fibers terminate in the cochlear nucleus (CN). From there, at least five distinct neural pathways are initiated; these pathways ascend through a multitude of other brainstem nuclei including the superior olive (SO) and the nuclei of the lateral lemniscus (NLL) before converging upon the inferior colliculi (IC). The colliculi then provide most, if not all, of the input to the auditory thalamus (MGB) and cortex (A1).
The auditory system is unique among the sensory modalities in that it has more than one nucleus between the peripheral sensors and the thalamocortical system. This suggests that substantial signal processing occurs in these brainstem nuclei. The long-term goals of our research are to determine the roles of these various nuclei in audition using a variety of engineering and quantitative physiological approaches. hese approaches include single- and multi-unit recording and analysis techniques, pharmacological manipulations, and computer modeling studies.
Classification of single units
Physiological classification of single units is a first step in understanding the neural processing of acoustic information that occurs in a nucleus. One classification scheme, called the response map scheme, is based on the relative prominence of a neuron′s excitatory and inhibitory responses to pure tones (see demo on the right). To see how different neurons in the dorsal cochlear nucleus respond to tones, click on either the principal output (P) or the vertical cell (V) to place the electrode to the cell′s body. To see auditory nerve (AN) response map click on the auditory nerve fiber. Initially the electrode is positioned on the principal (P) cell. The red (blue) area in the map indicates stimulus conditions which cause the neuron to show excitatory (inhibitory) responses to tones. Click different places in the response map to change the frequency and intensity of the tonal stimulus and observe the resultant activity in the model to the right. Note that when the frequency is in excitatory range and the level is just above AN threshold the P cell responds (produces spikes). However, when the level goes to a higher value, the V cell starts to fire and the P cell turns off. |
Functional Pathways in The Inferior Colliculus
Current research in the laboratory centers on the central nucleus of the inferior colliculus (ICC) because it occupies a pivotal position in the central auditory system; it receives direct inputs from most, if not all, of the auditory nuclei in the brainstem and, in turn, provides nearly all of the input to the auditory forebrain. Anatomical evidence suggests that the projections to the ICC form highly organized synaptic domains with both segregated and shared sources of input. In support of this parallel processing model, our recent electrophysiological studies have discovered that ICC units can grouped into three major types based on the patterns of excitation and inhibition evoked by contralateral tones of differing frequency and level. Examples of these ICC response types, labeled type V, I, and O, based on the shape of their excitatory response areas (red fill), are shown below. Several lines of experimental evidence lead to the conjecture that these response types reflect a dominant excitatory input from the medial superior olive, the lateral superior olive, or the dorsal cochlear nucleus. We are now performing experiments designed to provide direct evidence for these connections.
Processing of sound localization cues
In addition to investigations directed towards describing the anatomical pathways that link the auditory mid brain to the brainstem, the laboratory is also exploring the functional consequences of this synaptic organization by comparing the quality of acoustic representations in inferior colliculus (ICC) target neurons and their sources of input. A question of particular interest in these latter experiments is how the ascending inputs to the ICC interact with each other and a rich intrinsic inhibitory circuitry to enhance the processing of sound localization information.
Human psychophysical experiments have established that three main acoustic cues contribute to our ability to localize sounds in space: interaural differences in time and intensity, and spectral cues. The first two cues arise when a sound from one side of the head reaches the opposite ear delayed in time and attenuated in level with respect to that sound reaching the near ear. The third cue, spectral information, is created by the filtering properties of the head and outer ear as auditory stimuli propagate to the eardrum. Multiple lines of evidence suggest that these three cues are processed in largely parallel neural pathways in the brainstem and that this information remains functionally segregated at the level of the ICC. We are now performing experiments to test this hypothesis.
Computational models
There are few conceptual models of the neural circuitry in the inferior colliculus. One such model involving a pathway from the dorsal cochlear nucleus to the inferior colliculus is shown to the right. This model suggests that the response properties of type O units are due, in part, to inputs from the dorsal cochlear nucleus (IV), an inhibitory source (INH) and a wideband excitatory source (WBE). In turn, type IV units receive excitatory input from auditory nerve fibers and inhibitory input from I2 (vertical) cells and wibeband inhibitors (W-cells). A computational model based on this conceptual model has now been implemented and we are now performing simulations to determine if this model can account for the response properties of type O units. |
References
Figures adapted from the following references:
- SILVERSTEIN, H., WOLFSON, R. J., AND ROSENBERG, S. Clinical Symposia: Diagnosis and Management of Hearing Loss, edited by Erdélyi-Brown M, Craig JA, and Bean KJ. New Jersey: CIBA-GEIGY Corp, 1992, vol. 44(3).
- OSEN, K. K. AND MUGNAINI, E. Neuronal circuits in the dorsal cochlear nucleus. In: Neuronal Mechanisms of Hearing, edited by Syka J and Aitkin L. New York: Plenum, 1981, p. 119-125.
- RAMACHANDRAN, R., DAVIS, K. A., AND MAY, B. J. Single-unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps. J. Neurophysiol. 82: 152-163, 1999.
- MOORE, B. C. J. Psychology of Hearing. California: Academic Press, 1997.