Duration selective neurons in the inferior colliculus of the rat: topographic distribution and relation of duration sensitivity to other response properties.

Many animals use duration to help them identify the source and meaning of a sound. Duration-sensitive neurons have been found in the auditory midbrain of mammals and amphibians, where their selectivity seems to correspond to the lengths of species-specific vocalizations. In this study, single neurons in the rat inferior colliculus (IC) were tested for sensitivity to sound duration. About one-half (54%) of the units sampled showed some form of duration selectivity. The majority of these (76%) were long-pass neurons that responded to sounds exceeding some duration threshold (range: 5-60 ms). Band-pass neurons, which only responded to a restricted range of durations, made up 13% of duration-sensitive neurons (best durations: 15-120 ms). Other units displayed short-pass (2%) or mixed (9%) response patterns. The majority of duration-sensitive neurons were localized outside the central nucleus of the IC, especially in the dorsal cortex, where more than one-half of the neurons sampled had long-pass selectivity for duration. Band-pass duration tuned neurons were only found outside the central nucleus. Characteristics of duration-sensitive neurons in the rat support the idea that this filtering arises through an interaction of excitatory and inhibitory inputs that converge in the IC. Band-pass neurons typically responded at sound offset, suggesting that their tuning is created through the same mechanisms that have been described in echolocating bats. The finding that the first-spike latencies of all long-pass neurons were longer than the shortest duration to which they responded supports the idea that they receive transient inhibition before, or simultaneously with, a sustained excitatory input. The ranges of selectivity in rat IC neurons are within the range of durations of rat vocalizations. These data suggest that a population of neurons in the rat IC have evolved to transmit information about behaviorally relevant sound durations using mechanisms that are common to all mammals, with an emphasis on long-pass tuning characteristics.

Relation between intrinsic connections and isofrequency contours in the inferior colliculus of the big brown bat, Eptesicus fuscus.

Information processing in the inferior colliculus depends on interactions between ascending pathways and intrinsic circuitry, both of which exist within a functional tonotopic organization. To determine how local projections of neurons in the inferior colliculus are related to tonotopy, we placed a small iontophoretic injection of biodextran amine at a physiologically characterized location in the inferior colliculus. We then used electrophysiological recording to place a grid of small deposits of Chicago Sky Blue throughout the same frequency range to specify an isofrequency contour. Using three-dimensional computer reconstructions, we analyzed patterns of transport relative to the physiologically determined isofrequency contour to quantify the extent of the intrinsic connection lamina in all three dimensions. We also performed a quantitative analysis of the numbers of cells in different regions relative to the biodextran amine injection. Biodextran amine-labeled fibers were mainly located dorsomedial to the injection site, confined within the isofrequency contour, but biodextran amine-labeled cells were mainly located ventrolateral to the injection site. When we counted numbers of labeled cells classified by morphological type, we found that both elongate and multipolar cells were labeled within the isofrequency contour. Because the dendrites of multipolar cells typically extend outside the isofrequency lamina, it is likely that they receive input from other isofrequency contours and relay it to more dorsomedial portions of their specific isofrequency contour, along with the frequency-specific projections of the elongate cells. Within a given isofrequency contour, there is a consistent organization in which intrinsic connections ascend from the ventrolateral portion to more dorsomedial points along the contour, forming a cascaded system of intrinsic feedforward connections that seem ideally suited to provide the delay lines necessary to produce several forms of selectivity for temporal patterns in inferior colliculus neurons.

Frequency tuning properties of neurons in the inferior colliculus of an FM bat.

We examined frequency tuning characteristics of single neurons in the inferior colliculus of the echolocating bat, Eptesicus fuscus, in order to determine whether there are different classes of spectral selectivity at this level and to relate frequency tuning properties to the design of the echolocation signal. In unanesthetized but tranquilized animals, we recorded responses from 363 single units to pure tones, frequency-modulated (FM) sweeps, or broad-band noise. Most units were selective for stimulus type; 50% responded only to pure tones, 14% responded only to FM sweeps, and 5% responded only to noise. The remainder responded to two or more types of stimuli. Tuning curves could be classified as follows: 1) V-shaped tuning curves (57%) were the most common type; 2) closed tuning curves (20%) had thresholds at both low and high sound levels; 3) narrow filters (14%) had Q values above 20 at 10 dB and 30 dB above threshold or 10 dB and 40 dB above threshold; 4) frequency-opponent tuning (6%) was found in units with high spontaneous activity; within a center range of frequencies, firing rate increased above spontaneous level, but at higher or lower frequencies, firing rate decreased below spontaneous level; 5) double-tuned units (3%) had two best frequencies (BF). The most clear evidence of topographic distribution was seen for filter units, which were only found in the dorsal part of the 20-30 kHz isofrequency contour. Filter units were also the most clearly related to the echolocation signal of the bat. Their BFs were all within the range of the dominant frequency (approximately 20-30 kHz) that Eptesicus uses during the searching phase of echolocation.

Central acoustic tract in an echolocating bat: an extralemniscal auditory pathway to the thalamus.

To determine the sources and targets of auditory pathways that bypass the inferior colliculus in the mustache bat, we injected WGA-HRP in the medial geniculate body and related auditory nuclei of the thalamus as well as in the lower brainstem. We used electrophysiological methods to verify that the injection electrode was in an area responsive to sound. The only thalamic injections that produced retrograde transport to cells in auditory nuclei caudal to the inferior colliculus were those that included the suprageniculate nucleus. These injections labeled a group of large multipolar cells lying between the ventral nucleus of the lateral lemniscus and the superior olivary complex. Neurons in this cell group have also been shown to project to the deep layers of the superior colliculus in the mustache bat. The pathway revealed by these studies is almost identical to the "central acoustic tract" in which fibers course medial to the lateral lemniscus and bypass the inferior colliculus to reach the deep superior colliculus and the suprageniculate nucleus.