Gary J. Rose

Short-term synaptic plasticity as a temporal filter

Synaptic efficacy can increase (synaptic facilitation) or decrease (synaptic depression) markedly within milliseconds after the onset of specific temporal patterns of activity. Recent evidence suggests that short-term synaptic depression contributes to low-pass temporal filtering, and can account for a well-known paradox - many low-pass neurons respond vigorously to transients and the onsets of high temporal-frequency stimuli. The use of depression for low-pass filtering, however, is itself a paradox; depression induced by ongoing high-temporal frequency stimuli could preclude desired responses to low-temporal frequency information. This problem can be circumvented, however, by activation of short-term synaptic facilitation that maintains responses to low-temporal frequency information. Such short-term plasticity might also contribute to spatio-temporal processing.

Processing amplitude-modulated sounds by the auditory midbrain of two species of toads: matched temporal filters

Summary1.Recordings were made from single units in the torus semicircularis ofBufo americanus andBufo fowleri. Using sinusoidally amplitude-modulated (AM) white noise as a stimulus, the temporal selectivity of these neurons could be described by five response categories: ‘AM nonselective’ (40%); ‘AM high-pass’ (8%); ‘AM low-pass’ (9%); ‘AM band-suppression’ (9%); and ‘AM tuned’ (34%).2.The degree to which the stimulus modulation rate was coded in the periodicity of spiking of each toral neuron (i.e., synchronization of a units spikes to a particular phase of the modulation waveform) was calculated for modulation rates ranging from 10 to 150 Hz. The synchronization characteristics of toral neurons generally failed to reveal the temporal selectivity of these cells. In fact, those units which were most sharply AM-tuned rarely exhibited significant response synchronization at any modulation rate tested.3.The distribution of ‘best rates of AM’ is different for the two species of toads; AM-tuned neurons recorded from the torus semicircularis of Fowlers toad were, on the average, tuned to higher rates, relative to those recorded from the American toad. These findings constitute positive evidence for the existence of ‘matched temporal filters’ in the anuran central auditory system.4.Synthetic stimuli differing only in the rate at which they were amplitude modulated were used to evoke advertisement calls from maleBufo americanus. Modulation rates of 7.5 Hz, 15 Hz, 30 Hz, 60 Hz and 120 Hz were used. In these field studies males responded best to 30 Hz AM; lower or higher modulation rates were less effective. The AM-tuned neurons in the torus semicircularis of this species are well suited to process AM rates of 30 Hz.

Activation of Mauthner neurons during prey capture

The Mauthner (M-) cells, a bilateral pair of medullary neurons in fish, initiate the characteristic “C-start” predatory escape response of teleosts. Similar movements have been described during hatching, social interactions, and feeding. M-cell firing, however, has not been correlated directly with these other behaviors. The objective of this study was to determine whether the M-cell, in addition to escape, plays a role in feeding.1.Goldfish were chronically implanted with electrodes positioned near the axon cap of one of the two M-cells. Subsequently, M-cell activity was monitored for up to 8 days while fish were surface feeding on live crickets.2.The M-cell fires and the fish performs a C-shaped flexion in association with the terminal phase of prey capture. Thus, the M-cell is active in the context of at least two behaviors, predator escape and prey capture, and may be considered a part of behaviorally shared neural circuitry.3.For the goldfish, Mauthner-initiated flexions during feeding rapidly remove the prey from the waters surface and minimizes the fishs own susceptibility to surface predation. Other species may possess a diverse repertoire of Mauthner-mediated feeding behaviors that depend on their adaptive specializations for predation. Moreover, group competition between predators and their prey may have facilitated a “neural arms race” for M-cell morphology and physiology.

Long-term temporal integration in the anuran auditory system

Analysis of the temporal structure of acoustic signals is important for the communication and survival of a variety of animals including humans. Recognition and discrimination of particular temporal patterns in sounds may involve integration of auditory information presented over hundreds of milliseconds or seconds. Here we show neural evidence for long-term integration in the anuran auditory system. The responses of one class of auditory neurons in the torus semicircularis (auditory midbrain) of frogs reflect the integration of information, gathered over approximately 45–150 ms, from a series of stimulus pulses, not stimulus energy. This integration process is fundamental to the selective responses of these neurons for particular call types.

Effects of serotonergic lesions on investigatory responding by rats in a holeboard

Both the frequency and the typical durations of nose pokes by rats (male Sprague-Dawleys) into holes in the floor during a 24-min session in a holeboard were markedly increased by electrolytic lesions of the median raphe nucleus, and only slightly increased by lesions of the dorsal raphe nucleus. The raphe lesion-induced augmentation of holeboard responding was evident both 5 and 21 days after surgery, although a significant attenuation of the effect was found in the latter test. These lesions reduced hippocampal and striatal serotonin, respectively. However, comparable depletions of forebrain serotonin produced by infusions of the neurotoxin, 5,7-dihydroxytryptamine, into the lateral ventricle (100 μg/10 μl), the hippocampus (45 μg/4.5 μl each side), or the median raphe nucleus (3 μg/0.3 μl) had no significant effect on behavior in the holeboard. Furthermore, the neurotoxin was ineffective in affecting holeboard responding in the same animals in which hyperreactivity was demonstrable in a tactile startle test. These results suggest that the effects of electrolytic raphe lesions on behavioral measures of reactivity are better related to depletions of forebrain serotonin than are the effects of these lesions on measures of activity or investigatory behavior. An additional experiment demonstrates that the reductions in holeboard responding produced by either the hallucinogen, d-lysergic acid diethylamide (100 μg/kg), or the dopaminergic agonist, apomorphine (1.0 mg/kg), are unaltered by either electrolytic or neurotoxic lesions of the ascending serotonergic pathways. Therefore, the effects of these drugs on investigatory responses in a holeboard appear to be independent of their effects on central serotonergic systems.

Neural coding of difference frequencies in the midbrain of the electric fishEigenmannia: Reading the sense of rotation in an amplitude-phase plane

SummaryEigenmannia is able to discriminate the sign of the difference, Df, between the frequency of a neighbors electric organ discharge (EOD) and that of its own EOD. This discrimination can be demonstrated at the level of individual neurons of the midbrain. Intracellular and extracellular recordings of such sign-selective cells revealed the following:1.Units preferring positive Dfs and units preferring negative Dfs were found with equal frequency. The degree of selectivity was also similar for these two classes of neurons.2.All sign-selective units were sensitive to the magnitude of the frequency difference, i.e. the beat rate. Most units responded best to beat rates in the 4–8 Hz range.3.Sign-selectivity was observed only when the jamming signal (S2) was presented through electrodes other than those used to deliver the mimic (S1) of the fishs EOD, i.e. only when amplitude modulations were accompanied by modulations of differential phase.4.Intracellular studies suggest that most signselective neurons of the tectum are large, multipolar cells in the stratum album centrale. These cells send projections to the reticular formation, to lamina 9 of the torus semicircularis and to the N. electrosensorius.

Counting on Inhibition and Rate-Dependent Excitation in the Auditory System

The intervals between acoustic elements are important in audition. Although neurons have been recorded that show interval tuning, the underlying mechanisms are unclear. The anuran auditory system is well suited for addressing this problem. One class of midbrain neurons in anurans responds selectively over a narrow range of pulse-repetition rates (PRRs) and only after several sound pulses have occurred with the “correct” timing. This “interval-counting” process can be reset by a single incorrect interval. Here we show, from whole-cell patch recordings of midbrain neurons in vivo, that these computations result from interplay between inhibition and rate-dependent excitation. An individual pulse or slowly repeated pulses elicited inhibition and subthreshold excitation. Excitation was markedly enhanced, however, when PRR was increased over a neuron-specific range. Spikes were produced when the enhanced excitation overcame the inhibition. Interval-number thresholds were positively correlated with the strength of inhibition and number of intervals required to augment the excitation. Accordingly, interval-number thresholds decreased when inhibition was attenuated by loading cells with cesium fluoride. The selectivity of these neurons for the interpulse interval, and therefore PRR, was related to the time course of excitatory events and the rate dependence of enhancement; for cells that were tuned to longer intervals, EPSPs were broader, and enhancement occurred at slower PRRs. The frequency tuning of the inhibition generally spanned that of the excitation, consistent with its role in temporal computation. These findings provide the first mechanistic understanding of interval selectivity and counting in the nervous system.

NEW TECHNIQUES FOR MAKING WHOLE-CELL RECORDINGS FROM CNS NEURONS IN VIVO

Abstract Patch-type pipettes increasingly are being used to obtain intracellular ‘whole-cell’ recording from neurons. Here we describe our methods for making whole-cell recordings in vivo from midbrain neurons in an electric fish. Novel elements in the procedure are: A device for micropositioning the pipette when near a cell use of a ‘Picospritzer’ for cleaning the pipette tip and cell surface, and an electroporetic method, for perforating the patch following seal formation. In addition, we show that extracellular and intracellular recordings can be made from the same neuron. Stable intracellular recordings can be made from neurons at least as small as 10 μm.

Hierarchical Sensory Guidance of Mauthner-Mediated Escape Responses in Goldfish (Carassius auratus) and Cichlids (Haplochromis burtoni)

Acoustically-evoked escape behaviors were compared between goldfish (Carassius auratus), a hearing specialist, and the cichlid Haplochromis burtoni, a hearing nonspecialist. Fish were startled with compressive and rarefying, stimuli presented alone or together, and with compressive pulses preceded by a visual cue or after exposure to cobalt, an inhibitor of lateral line-innervated neuromast hair cells. These acoustic startle stimuli can evoke Mauthner neuron firing and are similar to but weaker than those produced by a largemouth bass (Micropterus salmoides) feeding on guppies. When sound stimuli were presented alone, both species avoided the direction of either the compressive or rarefying stimulus. If a light preceded and was contralateral to the compressive sound pulse, goldfish continued to avoid the sound source; cichlids avoided the visual cue and turned toward the sound. Goldfish performance improved significantly when the visual cue was in the same direction as the sound source. Goldfish performance also improved significantly after exposure to 0.1 mmol l-1 cobalt solution for 24 hours before testing, but cichlids would not startle after cobalt acclimation. A compressive pulse presented to one side of a fish simultaneously with a rarefying pulse on the other side causes the entire fish to accelerate with the water current. This strongly and directly accelerates the ear but tends to reduce both the pressure changes transduced by the swimbladder and activation of the mechanosensory lateral line. In this test, goldfish reliably avoided the compressive pulse. Cichlids, however, randomly avoided either speaker polarity but significantly avoided the speaker which had a faster onset. With more closely matched speakers, cichlids also preferentially avoided the compressive stimulus. Thus, the primitive sensory condition for auditory activation and guidance of Mauthner-neuron-initiated escape responses may have evolved to detect the initially compressive sounds associated with ram-type predators.

'Recognition units' at the top of a neuronal hierarchy? - Prepacemaker neurons in Eigenmannia code the sign of frequency differences unambiguously

SummaryThe electric fish,Eigenmannia, is able to discriminate the sign of the frequency difference, Df, between a neighbors electric organ discharges (EODs) and its own. The fish lowers its EOD frequency for positive Dfs and raises its frequency for negative Dfs to minimize jamming of its electrolocation ability by a neighbors EODs of similar frequency. This jamming avoidance response (JAR) is controlled by a group of ‘sign-selective’ neurons in the prepacemaker nucleus (PPN) that is located at the boundary of the midbrain and the diencephalon (Fig. 1). Extracellular recordings from a total of 35 neurons revealed a great similarity between behavioral and neuronal response properties:1.All neurons fired vigorously for negative Dfs and were almost silent for positive Dfs, regardless of the orientation of the jamming stimulus, and thus discriminated the sign of Df unambiguously (Fig. 2).2.In accordance with behavioral observations, individual neurons failed to discriminate the sign of Df when the jamming stimulus had the same field geometry as the signal mimicking the animals own EOD (Fig. 3).3.Df magnitudes which evoke strongest JARs, usually 4 to 8 Hz, also induced most vigorous responses in sign-selective neurons (Fig. 5).4.Behavioral and neuronal thresholds for the detection of small jamming signals were similar. Threshold for sign selectivity was reached when the amplitude ratio of the jamming signal to the EOD mimic, measured near the head surface, was 0.001. This value corresponds to a maximal temporal disparity (a necessary cue for performing a correct JAR) of 1 to 2 μs for signals received by the two sides of the body in a transverse jamming field (Fig. 7).5.The effects of two jamming fields, offered orthogonally to each other, may interact nonlinearly at the behavioral as well as at the neuronal level. A positive Df presented in one field may suppress behavioral and neuronal responses to modulations of the sign of Df in the other field (Fig. 8c).