Encoding of sound motion by binaural brainstem units in a Horseshoe bat

Abstract

In order to study how and if single brainstem units respond to moving compared with stationary sounds, radially moving sound sources were presented to the bat, Rhinolophus ferrumequinum. This time-variant binaural stimulation was simulated dichotically through earphones (closed-acoustic-field for the virtual azimuth range of ±40° from the midline). Neurophysiologically recorded responses primarily showed a function of interaural intensity difference (IID) which is considered a direct correlate of the sound source's azimuth angle. However, this is only true for the stationary case. Unit's response did not remain unaffected by the dynamic stimulus cues of sound source movement (velocity and direction). Maximal discharge rate became a function of motion velocity as well as the slopes of the response profiles. Hence, coding of IID became ambiguous as, depending on the unit, the response profiles and therefore a unit's receptive field, became spatially shifted with respect to one another when the direction of the sound source movement was reversed. Shifts within the movement direction (hysteresis) as well as against it (termed here ‘advance’) were observed: hysteresis is typical for units with non-monotonic, stationary rate/intensity functions, whereas those units with monotonic functions predominantly show advances. Further dynamic response features in form of transient peaks and troughs, superimposed on the response profiles, were registered. It appears that the ongoing firing rate no longer represents azimuth position alone, but vigorously reproduces the dynamic cues (velocity and movement direction), too. With respect to the neural mechanisms leading to dynamic response features, it is proposed that, as long excitation and inhibition act with similar short time constants, neural activity can rapidly and faithfully follow changing IIDs. Different time constants for excitation, inhibition, facilitation, and depression may be responsible for the dynamic ‘features’ such as transient responses and hysteresis/advance. They may provide biologically relevant information for nocturnally hunting bats to efficiently guide their flight maneuvers.

Introduction

Early studies of binaural interaction were concerned with how single units encode interaural disparities and, indirectly, horizontal sound locations (azimuth). Interaural level (ILD) or intensity difference (IID) is one of the two relevant physical parameters for azimuth analysis. Binaural mechanisms acting with excitation from one side and inhibition from the other (termed I/E or E/I) are best suited to code for IID and, hence indirectly, azimuth. This concept became neurophysiologically well confirmed (e.g. Rose et al., 1969, Guinan et al., 1972). These investigations delt with stationary stimulus conditions and described how neurons code for real (in the free-acoustic-field) or virtual (closed-acoustic-field) sound locations. However, some older, and a considerable number of more recent, neurophysiological studies found feature-specialized neurons for sound motion at binaural brainstem levels and up to the cortex (e.g. Ahissar et al., 1992, Altman, 1968, Altman and Viskov, 1977, Doan and Saunders, 1999, Jiang et al., 2000, Schlegel, 1979a, Schlegel, 1979b, Schlegel et al., 1988, Sovijärvi et al., 1973, Sovijärvi and Hyvärinen, 1974, Spitzer and Semple, 1993, Takahashi and Keller, 1992, Toronschuk et al., 1992, Wagner, 1990, Wagner and Takahashi, 1990, Wagner and Takahashi, 1992, Wilson and O'Neill, 1991, Wilson and O'Neill, 1998; review by Wagner et al., 1997). Hence, these units’ responses were influenced by time-variant (=dynamic) cues, i.e. real or virtual sound source motion.

It is important to establish whether or not a particular IID elicits the same neural activity when presented stationary or when that same IID is reached while binaural combinations are being varied over time: time-dependent monaural and binaural integrative processes are expected to show up in the ‘response profiles’ (neural activity as a function of IID). Neural responses and receptive fields are, presumably, not only affected by IIDs but also by the neuron's recent history (compare e.g. Ingham et al., 2001, Kleiser and Schuller, 1995, Sanes et al., 1998, Spitzer and Semple, 1993, Firzlaff and Schuller, 2001). Are dynamic cues reproduced as features for movement velocity and direction by the neural activity? The binaural model seems especially suited to analyzing time-dependent neural processes. In the present study, IID-changes were introduced dichotically, thus mimicking horizontal sound source movements between virtually ±40°. Responses to stationary and dynamic IID stimuli were compared for individual units at the binaural brain-stem levels.

Biologically, targets moving across a bat's flight path (reflected echoes from insects) or active rotations of the bat's head can create important and rapid changes in IID (Grinnell, 1970, Grinnell and Hagiwara, 1972, Schlegel, 1977a, Schlegel, 1979a, Schlegel, 1979b, Shimozawa et al., 1974) and are likely to be biologically relevant stimulus parameters which are processed by the auditory system. The velocities concerned may be estimated as ranging below about 50°/s (although not studied in detail in most investigations) but could reach 500–1500°/s in extreme cases, e.g. when bats are catching up to four insects per second (Griffin, 1958). Neurally processed information on movements of targets would therefore be particularly useful for flight control.