Characterisation of Brainstem Lateral Line Neurons in Goldfish, <em>Carassius auratus</em>

Abstract

In the present study lateral line units in the medial octavolateral nucleus (MON) in the brainstem in goldfish, Carassius auratus, were extracellulary recorded. The aim of the work was to investigate and characterize the response behaviour of these units to different hydrodynamic stimuli to learn more about central processing of lateral line information. It was investigated how MON units respond to a vibrating sphere in terms of different frequencies, locations, and sphere vibration directions. The spatial excitation patterns of Mon units were described and finally the response behaviour to water flow in different directions and velocities.<br /> The responses of MON units to a vibrating sphere presented with various vibration frequencies were analyzed and described. Most of the units exhibited a change in discharge rate and/or phase-locking to at least one of the applied stimulation frequencies (90.4 %). Three groups of units were distinguished. Units from Group 1 (9.6 %) responded with a change in discharge rate and/or a phase coupling to only one, units from Group 2 responded to two (25.5 %), and units from Group 3 (55.3 %) responded to all three applied stimulation frequencies. Eighty-six out of ninety-four units responded to any of the applied frequencies with an increase or a decrease in discharge rate and/or with phase coupling. Eight units did not respond to any of the presented stimuli. The current findings demonstrate that response behaviour, patterns of discharge and frequency response characteristics of brainstem lateral line units are much more diverse than those of primary afferents. Most MON units responded preferentially to one particular stimulus frequency. 45 % of the units showed their strongest response in terms of discharge rate (increase or decrease) and/or phase locking to the 50 Hz stimulus, 42 % in response to 100 Hz, and 13 % to 20 Hz. Thus, many MON units exhibited band-pass, high-pass, or low-pass characteristics.<br /> Theoretical data suggest that information on the position of a vibrating source is linearly coded in the spatial characteristics of the excitation pattern of pressure gradients distributed along the lateral line (Curcic-Blake and van Netten 2006). The theoretical predictions were confirmed by neurophysiologic experiments performed on single fibres in the posterior lateral line nerve of goldfish, demonstrating that the location and separation of peaks and troughs in the neuronal responses change in a predictable way with location and vibration angle of a dipole, i.e., sinusoidally vibrating sphere. If a central unit would receive input from peripheral receptors then this central unit would directly encode for object location. It was searched for such units in medial octavolateralis nucleus in the fish brainstem by systematically investigating spatial excitation properties with a sinusoidally vibrating sphere. Spike activity evoked by the sphere was recorded as function of sphere location alongside the fish and different angles of sphere vibration (0°=parallel to the fish, 90°=perpendicular to the fish, 45° and 135°). The current data show that MON units exhibit very variable spatial excitation patterns. Excitation patterns with single excitatory or inhibitory areas were found as well as excitation patterns with two or more excitatory or inhibitory areas. Further excitation patterns exhibited broad areas of increased or decreased discharge rate along a big part of the fish’s body as response to stimulation. The observed effects were different from those predicted for primary afferent fibres. Units with a distinct stimulation direction preference were not observed. Nevertheless, most of the MON units showed different responses to the given vibration directions. The changes were not that regularly or predictable like in primary afferent fibres. In most of the units the generally shape of their excitation patterns stayed nearly stable at the different vibration directions. The differences insisted in shifts of the excitation patterns flanks. Some other units changed number or location of the response peaks. These data suggest that pressure gradient patterns are not represented by MON units as they are by the lateral line periphery. This implies that information about the sinusoidally vibrating sphere may be inferred from brainstem excitation patterns. For the first time is shown that there are effects of sphere vibration angle on the excitation pattern shape and size on lateral line units in the fish brainstem.<br /> Literature suggests that fluctuations within a water flow may be used to determine flow direction and flow velocity by comparing inputs from an array of peripheral receptors. To test, this hypothesis, we recorded the activity from brainstem units in response to water flow. We analyzed the response characteristics with special respect to directional sensitivity to flow passing the fish from anterior to posterior and opposite, i.e. from posterior to anterior. If brainstem units indeed determine flow velocity and flow direction by comparing inputs from two or more neuromasts that are organized in series on the fish surface, then units should be found that respond preferentially to particular flow velocities and flow directions. The spike activity of brainstem units in response to different constant flow velocities and continuously rising flow was systematically investigated. The data show that different MON units can exhibit quite variable responses to water flow. Moreover, most responses were different from those described for primary afferent fibres. Units were found that responded with an increase in discharge rate to both flow directions, with a decrease in both directions and units that exhibit an increase and/or decrease depending on flow direction. Units with a clear preference for a distinct flow velocity, i.e., units that responded only to a particular flow velocity, were not found. A few units differed in their responses to the presented flow directions. However, MON units apparently do not encode water velocities and directions in the same way as primary lateral line afferent fibres.