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E S Fortune

Publications and source records attributed to E S Fortune.

13 recordsLinked to original sources

Global electrosensory oscillations enhance directional responses of midbrain neurons in eigenmannia.

Eigenmannia, a genus of weakly electric fish, exhibits a specialized behavior known as the jamming avoidance response (JAR). The JAR results in a categorical difference between Eigenmannia that are in groups of conspecifics and those that are alone. Fish in groups exhibit the JAR behavior and thereby experience ongoing, global synchronous 20- to 50-Hz electrosensory oscillations, whereas solitary fish do not. Although previous work has shown that these ongoing signals do not significantly degrade electrosensory behavior, these oscillations nevertheless elicit short-term synaptic depression in midbrain circuits. Because short-term synaptic depression can have profound effects on the transmission of information through synapses, we examined the differences in intracellularly recorded responses of midbrain neurons in awake, behaving fish to moving electrosensory images under electrosensory conditions that mimic solitary fish and fish in groups. In solitary conditions, moving objects elicited Gaussian or sinusoidal postsynaptic potentials (PSPs) that commonly exhibited preferential responses to a direction of motion. Surprisingly, when the same stimulus was presented in the presence of the global oscillations, directional selectivity was increased in all neurons tested. The magnitudes of the differences in PSP amplitude for preferred and nonpreferred directions were correlated with a measure of short-term synaptic depression in both conditions. The electrosensory consequences of the JAR appear to result in an enhancement of the representation of direction of motion in midbrain neurons. The data also support a role for short-term synaptic depression in the generation and modulation of directional responses.

Animals↗

Encoding and processing biologically relevant temporal information in electrosensory systems.

Wave-type weakly electric fish are specialists in time-domain processing: behaviors in these animals are often tightly correlated with the temporal structure of electrosensory signals. Behavioral responses in these fish can be dependent on differences in the temporal structure of electrosensory signals alone. This feature has facilitated the study of temporal codes and processing in central nervous system circuits of these animals. The temporal encoding and mechanisms used to transform temporal codes in the brain have been identified and characterized in several species, including South American gymnotid species and in the African mormyrid genus Gymnarchus. These distantly related groups use similar strategies for neural computations of information on the order of microseconds, milliseconds, and seconds. Here, we describe a suite of mechanisms for behaviorally relevant computations of temporal information that have been elucidated in these systems. These results show the critical role that behavioral experiments continue to have in the study of the neural control of behavior and its evolution.

Action Potentials↗

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.

Animals↗

Short-term synaptic plasticity contributes to the temporal filtering of electrosensory information.

Short-term synaptic depression and facilitation often are elicited by different temporal patterns of activity. Short-term plasticity may contribute, therefore, to temporal filtering by impeding synaptic transmission for some temporal patterns of activity and facilitating transmission for other patterns. We examined this hypothesis by investigating whether short-term plasticity contributes to the temporal filtering properties of midbrain electrosensory neurons. Postsynaptic potentials were recorded in response to sensory stimuli and to direct stimulation of afferents, in vivo. Stimulating afferents with pairs of pulses at a rate of 20 pairs/sec ["tetanus (20 Hz)"] induced PSP depression. This PSP depression was similar to that observed for electrosensory stimuli of the same temporal frequency. Analysis of PSPs elicited by a pair of pulses that preceded versus followed the tetanus revealed that PSP depression was caused by synaptic depression, not by a loss of facilitation. Behavioral studies indicate that fish can detect slow changes in signal amplitude (slow AM) in backgrounds of fast fluctuations. Correspondingly, midbrain neurons respond well to slow AM even in the presence of fast AM. In many neurons, facilitation enhanced responses to trains (8-10 pulses; 100 Hz) that represented activity patterns elicited by slow AM, despite induction of synaptic depression by a tetanus (20 Hz). The interplay between synaptic depression and facilitation, therefore, can act as a filter of temporal information. Some neurons that showed little facilitation nonetheless responded to low temporal-frequency information after induction of depression by fast information; this likely results from the convergence of inputs with different temporal filtering properties.

Animals↗

Frequency-dependent PSP depression contributes to low-pass temporal filtering in Eigenmannia.

This study examined the contribution of frequency-dependent short-term depression of PSP amplitude to low-pass temporal filtering in the weakly electric fish Eigenmannia. Behavioral and neurophysiological methods were used. Decelerations of the electric organ discharge frequency were measured in response to continuous and discontinuous electrosensory stimuli. Decelerations were strongest (median = 4.7 Hz; range, 3.5-5.9 Hz) at continuous beat rates of approximately 5 Hz and weakest (median = 0.4 Hz; range, 0.0-0.8 Hz) at beat rates of 30 Hz. Gating 20 or 30 Hz stimuli at a rate of 5 Hz, however, elicited decelerations that were sixfold greater than that of continuous stimuli at these beat rates (median = 2.6 Hz; range, 2.0-4.7 Hz for 30 Hz). These results support the hypothesis that short-term processes enhance low-pass filtering by reducing responses to fast beat rates. This hypothesis was tested by recording intracellularly the responses of 33 midbrain neurons to continuous and discontinuous stimuli. Results indicate that short-term depression of PSP amplitude primarily accounts for the steady-state low-pass filtering of these neurons beyond that contributed by their passive and active membrane properties. Previous results demonstrate that passive properties can contribute up to 7 dB of low-pass filtering; PSP depression can add up to an additional 12.5 dB (median = 4.5). PSP depression increased in magnitude with stimulus frequency and showed a prominent short-term component (t(1) = 66 msec at 30 Hz). Initial PSP amplitude recovered fully after a gap of 150 msec for most neurons. Remarkably, recovery of PSP amplitude could be produced by inserting a brief low-temporal frequency component in the stimulus.

Animals↗

Mechanisms for generating temporal filters in the electrosensory system.

Temporal patterns of sensory information are important cues in behaviors ranging from spatial analyses to communication. Neural representations of the temporal structure of sensory signals include fluctuations in the discharge rate of neurons over time (peripheral nervous system) and the differential level of activity in neurons tuned to particular temporal features (temporal filters in the central nervous system). This paper presents our current understanding of the mechanisms responsible for the transformations between these representations in electric fish of the genus Eigenmannia. The roles of passive and active membrane properties of neurons, and frequency-dependent gain-control mechanisms are discussed.

Animals↗

Passive and active membrane properties contribute to the temporal filtering properties of midbrain neurons in vivo.

This study examined the contributions of passive and active membrane properties to the temporal selectivities of electrosensory neurons in vivo. The intracellular responses to time-varying (2-30 Hz) electrosensory stimulation and current injection of 27 neurons in the midbrain of the weakly electric fish Eigenmannia were recorded. Each neuron was filled with biocytin to reveal its anatomy. Neurons were divided into two biophysically distinct groups based on their frequency-dependent responses to sinusoidal current injection over the range 2-30 Hz. Fourteen neurons showed low-pass filtering, with a maximum decline in the amplitude of voltage responses of >2.6 dB (X = 4.30 dB, s = 1.10 dB) to sinusoidal current injection. These neurons also showed low-pass filtering of electrosensory information but with larger maximum declines in postsynaptic potential amplitude (X = 9.53 dB, s = 3.34 dB; n = 10). These neurons had broad dendritic arbors and relatively spiny dendrites. Five neurons showed all-pass filtering, having maximum decline in the amplitude of voltage responses of <2.0 dB (X = 1.16 dB, s = 0.61 dB). For electrosensory stimuli, however, these neurons showed low-, band-, or high-pass filtering. These neurons had small dendritic arbors and few or no spines. Voltage-dependent "active" conductances were revealed in eight neurons by using several levels of current clamp. In four of these neurons, the duration of the voltage-dependent conductances decreased in concert with the period of the electrosensory stimulus, whereas in the other four neurons the duration of the voltage-dependent conductances was relatively short (<30 msec) and nearly constant across sensory stimulation frequencies. These conductances enhanced the temporal filtering properties of neurons.

Animals↗

Temporal filtering properties of ampullary electrosensory neurons in the torus semicircularis of Eigenmannia: evolutionary and computational implications.

Weakly electric fish have parallel electrosensory systems, the phylogenetically older ampullary system and the novel tuberous system. The tuberous system is an adaptation related to the evolution of active electrolocation. To examine the evolutionary relationship of the ampullary and tuberous systems, the temporal filtering properties of ampullary neurons in the dorsal torus semicircularis of Eigenmannia were studied. 'Whole-cell' recordings were made in vivo using patch-type pipettes. The responses of 19 neurons to sinusoidal electric signals (< 40 Hz) were recorded and the anatomy of these neurons demonstrated by injection of biocytin. All eight low-pass ampullary neurons had broad, relatively smooth post-synaptic potentials (psps) that at low frequencies nicely reflected the sinusoidal stimuli. These neurons had somata of 10-14 microns diameter and thick, spiny dendrites. Eight high-pass neurons were recorded, representing three physiological classes. The first class (3 neurons) had psps that roughly followed the sinusoidal time course of the stimulus; the psp morphology was similar to low-pass neurons. The second class had many small, fast, individual psps; their rate of occurrence varied with the stimulus. Finally, four neurons showed psps that were of constant width across stimulus frequencies. All three classes of high-pass neurons had small somata (8-10 microns diameter) with thin dendrites and either few or no spines. Some of these neurons had large varicosities on the dendrites. Three neurons had band-pass filtering properties: neurons that showed strong band-pass properties were morphologically similar to low-pass neurons. Comparisons of the temporal filtering, shapes of post-synaptic potentials, and anatomy of ampullary and tuberous neurons in the torus suggest that the circuitry for tuberous processing in the torus may have evolved as an elaboration or duplication of the ampullary system. The mechanisms underlying the low-pass filtering characteristics of tuberous neurons therefore appear to have predated the evolution of the tuberous system and to have served as a pre-adaptation for the evolution of the jamming avoidance response. In addition, these data support the hypothesis that spine density influences the temporal filtering properties of neurons.

Animals↗

New techniques for making whole-cell recordings from CNS neurons in vivo.

Patch-type pipettes increasingly are being used to obtain intracellular 'whole-cell' recordings 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 formulation. 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 microns.

Action Potentials↗

Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches (Taeniopygia guttata).

The structure and connectivity of the forebrain nucleus HVc, a site of sensorimotor integration in the song control system of oscine birds, were investigated in adult zebra finches. HVc in males comprises three cytoarchitectonic subdivisions: the commonly recognized central region with large and medium-sized darkly staining cells, a ventral caudomedial region with densely packed small and medium-sized cells, and a dorsolateral region with oblong cells and rows of cells. All three subdivisions project to area X and the robust nucleus of the archistriatum, with more complexity in the classes and distribution of cells than previously reported. In females, HVc is very small and has a cytoarchitecture distinct from that of the three male subdivisions. The structure of HVc in females treated with estradiol at 15 days of age is similar to male HVc. Tracer studies in males with fluorescent and biotinylated dextrans demonstrate non-topographic projections onto HVc that may carry auditory information, including type 1 and type 2 neurons in subdivisions L1 and L3 of the field L complex, a class of neurons in nucleus interface, nucleus uvaeformis, the caudal neostriatum ventral to HVc, and intrinsic HVc connections. These data are interpreted in terms of HVc's functional properties. Additionally, the neostriatum immediately ventral to HVc receives projections from field L, ventral hyperstriatum, and caudal neostriatum, and projects to a region surrounding RA and near to or into area X. The similarity of the connectivity of HVc and adjacent neostriatum suggests the possibility that they share a common origin.

Afferent Pathways↗

Distributed representation in the song system of oscines: evolutionary implications and functional consequences.

This paper reviews the organizational principles and implications that have emerged from the analysis of HVc, a forebrain nucleus that is a major site of sensory, motor, and sensorimotor integration in the song control system of oscine passerine birds (songbirds). Anatomical, physiological, and behavioral data support the conclusion that HVc exists within a hierarchically organized system with parallel pathways that converge onto HVc. The organization of HVc is distributed and redundant, and its outputs exhibit broad divergence. A similar pattern of connectivity exists for neostriatum adjacent to HVc. This and other data support the hypothesis that the song system arose from an elaboration or duplication of pathways generally present in all birds. Spontaneous and auditory response activity is strongly correlated throughout HVc, with auditory responses exhibiting strong temporal modulation in a synchronized fashion throughout the nucleus. This suggests that the auditory representation of song is encoded in the synchronized temporal patterns of activation, and that the predominant selectivity for the individual's own song that is observed for HVc neurons results from interactions of auditory input with central pattern generators for song. Most, or all HVc neurons are recruited during singing. The auditory response and motor recruitment properties of individual HVc neurons have no simple relationship, and the spontaneous activity in HVc may build up in the seconds preceding a song. To the extent HVc participates in perceptual phenomena associated with song, production and perception are not tightly linked in adults but may be linked by shared developmental processes during periods of sensorimotor learning.

Animals↗

Cytoarchitectonic organization and morphology of cells of the field L complex in male zebra finches (Taenopygia guttata).

The organization of the field L complex, a thalamorecipient auditory region in the telencephalon of birds, was examined in Nissl and Golgi preparations of male zebra finches (Taenopygia guttata). The field L complex comprises five cytoarchitectonic subdivisions: L1, L2a, L2b, L3, and L, although the border between L and L2b is not distinct. L2a is a plate extending dorsocaudally from the dorsal medullary lamina in the caudal neostriatum. L1 lies on the anterodorsal border and L3 lies on the posteroventral border of L2a. L, the area designated "field L" by Rose (J. Psychol. Neurol., 1914, 2:278-352), forms the medial and posterior borders of the field L complex. L2b is a thick band that forms the dorsal and dorsolateral boundary of the field L complex and is continuous with L medially. Nucleus interface (NIf) is a nucleus that lies between L2a and L1 near the lateral edge of the complex. The four types of Golgi stained neurons that occur in the zebra finch field L complex correspond to those described for the European starling (Sturnus vulgaris). Additionally, type 3 neurons are subdivided into "unoriented" neurons with spherical dendritic fields and "oriented" neurons with bipolar dendritic fields. NIf contains a distinct class of neurons that have large somata with both thick and thin spiny dendrites. The distribution of Golgi cell types between the subdivisions of the field L complex corresponds to the morphology of cells seen in Nissl material. Type 3 oriented cells are found almost exclusively within L2a. L3 has significantly greater numbers of the largest cells (type 1) and significantly smaller numbers of the smallest cells (type 4) than does L1. There are no significant differences in the distribution of Golgi stained cells between L2b and L.

Animals↗

Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc.

Song learning shapes the response properties of auditory neurons in the song system to become highly selective for the individual bird's own ("autogenous") song. The auditory representation of autogenous song is achieved in part by neurons that exhibit facilitated responses to combinations of components of song. To understand the circuits that underlie these complex properties, the combination sensitivity of single units in the hyperstriatum ventrale, pars caudale (HVc) of urethane-anesthetized zebra finches was studied. Some neurons exhibited nonlinear temporal summation, spectral summation, or both. The majority of these neurons exhibited low spontaneous rates and phasic responses. Most combination-sensitive neurons required highly accurate copies of sounds derived from the autogenous song and responded weakly to tone bursts, combinations of simple stimuli, or conspecific songs. Temporal combination-sensitive (TCS) neurons required either two or more segments of a single syllable, or two or more syllables of the autogenous song, to elicit a facilitated, excitatory response. TCS neurons integrated auditory input over periods ranging from 80 to 350 msec, although this represents a lower limit. Harmonic combination-sensitive (HCS) neurons required combinations of two harmonics with particular frequency and temporal characteristics that were similar to autogenous song syllables. Both TCS and HCS neurons responded much more weakly when the dynamical spectral features of the autogenous song or syllables were modified than when the dynamical amplitude (waveform) features of the songs were modified. These results suggest that understanding the temporal dynamics of auditory responses in HVc may provide insight into neuronal circuits modified by song learning.

Animals↗