Synthesising a neuronal map of auditory space

Each space-specific neuron in the owl's midbrain responds to stimuli delivered via the earphones only when both the time difference and the intensity difference fall within the range to which it is tuned. It is not excited by either the correct time difference alone or the correct intensity difference alone. Evidently, the receptive fields are formed by tuning of the neurons to specific combinations of time differences and intensity differences, which are coded separately by lower-order neurons. The initial separation takes place at the level of the earliest staging post of the auditory pathway in the brain, consisting of the two cochlear nuclei, the angular nucleus and the magnocellular nucleus.

The information available to the brain is coded in spikes generated by the sensory neurons of the owl's inner ear. Each of these auditory neurons responds to a particular frequency of sound, and the neurons produce their spikes at or near a particular point on the arriving sound wave. This latter property is called phase locking and it is important for measuring a sound's time of arrival accurately. The number of spikes generated on each occasion is proportional to the sound pressure level at the ear. Thus, the train of spikes travelling along each axon of the auditory nerve carries information about both the time of arrival and the intensity of a particular sound frequency. When it reaches the brain, each of these sensory axons divides into two branches; one enters the angular nucleus and the other enters the mag-nocellular nucleus.

The role played by these two nuclei is revealed by an ingenious experiment in which a tiny amount of local anaesthetic is injected into one of them so as to inactivate most of its neurons (Takahashi, Moiseff & Konishi, 1984). The responses of the space-specific neurons are then re-examined to see what changes have occurred. The results are clear cut: inactivation of the angular nucleus alters the responses of the space-specific neurons to interaural intensity differences without affecting their responses to time differences, and inactivation of the magnocellular nucleus alters the neurons responses to time differences without affecting their responses to intensity differences. When recordings are made from the interneurons in these two nuclei, their properties are found to be consistent with this result. Neurons of the magnocellular nucleus preserve the phase locking shown by the sensory neurons but are insensitive to changes in intensity, whereas the neurons in the angular nucleus are sensitive to intensity changes but do not show phase locking. Evidently, these two cochlear nuclei serve as neural filters, which pass along information about either time of arrival or intensity, but not both.

The first place in the auditory pathway at which information from both ears is compared is the lamina nucleus, which receives excitatory input from both the left and right magnocellular nuclei. It seems clear from the anatomy and physiology of the lamina nucleus that this staging post serves to measure interaural time differences. The laminar neurons are arranged

Medial Superior Olive Mso

Figure 6.5 A neuronal circuit for measuring interaural time differences in the barn owl, shown as a highly diagrammatic section through the brain. The left laminar nucleus receives excitatory input from both the left and right magnocellular nuclei, represented here by a single axon from each. When spikes conducted along the left and right magnocellular axons reach a given laminar neuron simultaneously, that neuron will be strongly excited. This will happen whenever the difference in a sound's arrival time at the two ears compensates for the difference in time taken for spikes to travel to that laminar neuron along the left and right magnocellular axons. (Modified after Konishi, 1992.)

Figure 6.5 A neuronal circuit for measuring interaural time differences in the barn owl, shown as a highly diagrammatic section through the brain. The left laminar nucleus receives excitatory input from both the left and right magnocellular nuclei, represented here by a single axon from each. When spikes conducted along the left and right magnocellular axons reach a given laminar neuron simultaneously, that neuron will be strongly excited. This will happen whenever the difference in a sound's arrival time at the two ears compensates for the difference in time taken for spikes to travel to that laminar neuron along the left and right magnocellular axons. (Modified after Konishi, 1992.)

in an elongated array, and the axons of the ipsilateral magnocellular neurons pass along this array from one end whereas the contralateral magnocellular axons pass along from the other end (Fig. 6.5). Both ipsilateral and contralateral axons give off terminal branches that make synaptic contact with the laminar neurons.

This circuit is able to compute interaural time differences on the principle of delay lines and coincidence detection. The laminar neurons fire maximally when they receive excitatory input simultaneously from both ipsilateral and contralateral magnocellular neurons and so function as coincidence detectors. The magnocellular axons function as delay lines because the time it takes each spike to travel along the axon from one end

Auditory Pathway Mso

Figure 6.6 A simplified flow diagram showing how the neuronal map of auditory space is synthesised in the brain of the barn owl. The boxes on the left represent successive regions of the brain, and the process that takes place in each region is shown on the right of the corresponding box. The arrows indicate the flow of information along pathways (left) and along the sequence of computational steps (right). Note the separation of the time and intensity pathways. (Modified after Konishi, 1992, 1993.)

Figure 6.6 A simplified flow diagram showing how the neuronal map of auditory space is synthesised in the brain of the barn owl. The boxes on the left represent successive regions of the brain, and the process that takes place in each region is shown on the right of the corresponding box. The arrows indicate the flow of information along pathways (left) and along the sequence of computational steps (right). Note the separation of the time and intensity pathways. (Modified after Konishi, 1992, 1993.)

of the lamina nucleus towards the other end causes a delay in the spike's time of arrival at a given laminar neuron. The point in the array of laminar neurons where the left and right magnocellular spikes arrive simultaneously will, therefore, vary systematically as a function of the difference in a sound's time of arrival at the left and right ears plus the conduction time along the magnocellular axons from the two ears. Consequently, for each frequency band, the array of laminar neurons effectively constitutes a neuronal map of interaural time differences (Carr & Konishi, 1990). The axons of the laminar neurons convey this information forward to the auditory midbrain, via the anterior part of the lateral lemniscal nucleus (Fig. 6.6).

The posterior part of the lateral lemniscus on each side of the brain receives axons directly from the contralateral angular nucleus. This input is excitatory and is in proportion to the sound pressure level at the contralateral ear. At the same time, each lateral lemniscus receives inhibitory input from the lemniscal nucleus on the opposite side of the brain and this reflects the sound pressure level at the ipsilateral ear. So the response of the lemniscal neurons depends on the balance between the degree of excitation and the strength of inhibition, which in turn depends on the intensity difference between the ears. Furthermore, the neurons of the posterior lateral lemniscus vary systematically in the intensity difference that causes them to respond maximally, forming a topographical array along the dorso-ventral axis (Manley, Koppl & Konishi, 1988). In effect, this array constitutes a neuronal map of interaural intensity differences for a given frequency band.

This information is passed along by the axons of the lemniscal neurons to the auditory midbrain, where it is eventually combined with the information on interaural time differences to generate the receptive fields of the space-specific neurons (Fig. 6.6). By this means, the neuronal map of auditory space is synthesised centrally from sensory cues that are not themselves spatially organised. The inner ear is organised tonotopically, with the topographical array of receptors coding frequency rather than space. For each frequency band, the ear monitors intensity and time of arrival, cues that are separated in the brain and processed in parallel pathways. In both pathways, the information from the left and right ears is brought together to form a topographical array of interaural differences. Finally, the intensity and time pathways are brought together, thereby enabling neurons in the auditory midbrain to encode specific combinations of time and intensity differences.

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