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1Departments of Psychological and Brain Sciences and 2Neuroscience, The Johns Hopkins University, Baltimore, Maryland
Submitted 22 March 2006; accepted in final form 15 June 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Cherry 1953; Feng and Ratnam 2000; Julesz and Hirsh 1972; Ronacher et al. 2000; Schiller 1965). Sources of noise include environmental stimuli arising from nonbiological sources, heterospecific sources, and, importantly, conspecifics. Competing signals generated by conspecifics can be particularly detrimental because the stimulus parameters of these interfering signals closely match the sensory tuning of the individual (Appeltants et al. 2005; Narins 1995; Ulanozsky et al. 2004).
Evolutionary processes have resulted in an array of solutions to this problem. For example, in social situations, humans can isolate single conversations from competing background conversations (Cherry 1953). This phenomenon is known as the "cocktail party effect." Another solution to this problem is found in certain species of weakly electric fishes. These fish exhibit a robust behavioral adaptation, the "jamming avoidance response" or JAR, which dramatically reduces detrimental sensory interference from nearby conspecific signals. This behavior has been best studied in the glass knife fish, Eigenmannia virescens (Heiligenberg 1991).
Eigenmannia produce weak electric fields, on the order of tens of millivolts, which are used in electrolocation and communication (Heiligenberg 1991). The electric fields are quasi-sinusoidal, and each fish maintains a nearly constant frequency within the range 200–700 Hz. When Eigenmannia are within about 1 m of each other, the electric fields of the fish mix, which results in "global" (broad-field) oscillating interference patterns at a rate equal to the frequency difference between the fish. These oscillating interference patterns, more commonly known as "beats," include both amplitude and phase modulations of the electric signal (Heiligenberg 1991). Oscillation rates between 3 and 8 Hz maximally impair both fish's ability to electrolocate, whereas oscillation rates of 
20 Hz do not (Bullock et al. 1972; Heiligenberg 1973). In the JAR, fish detect the detrimental oscillation rates, and the individual with the higher initial frequency raises its electrical frequency while the other fish lowers its frequency (Bullock et al. 1972; Watanbe and Takeda 1963). After the JAR has occurred, fish will experience ongoing global oscillations at rates typically between 20 and 50 Hz (Tan et al. 2005) as long as they remain in close proximity.
In the wild, Eigenmannia are most commonly found in close proximity to conspecifics (Tan et al. 2005). Given that alternate solutions to the electrosensory jamming problem exist, such as simply moving away from conspecifics or via other neural strategies (Matsubara 1981, 1982), we hypothesized that such oscillations in Eigenmannia might have specific computational consequences for electrosensory processing in the CNS. Indeed, previous studies demonstrated that global 20- to 50-Hz oscillations preferentially elicit short-term synaptic depression in midbrain electrosensory neurons (Fortune and Rose 2000; Rose and Fortune 1999). The dynamic responses of synapses that exhibit short-term synaptic depression, therefore, are expected to differ when fish are solitary versus when fish are in groups in which ongoing 20- to 50-Hz oscillations are generated as a result of the JAR. The changes in synaptic properties that are induced by the electrosensory signals that emerge as a result of the JAR behavior begs the question: how do these "background" signals affect the processing of salient signals, such as moving objects?
To determine whether 20- to 50-Hz global oscillations affect the processing of sensory signals in the nervous system, we made intracellular recordings from midbrain electrosensory neurons in awake, behaving Eigenmannia. We recorded the responses to a moving object in conditions that mimic a solitary Eigenmannia, and in the presence of global 20- to 50-Hz oscillations that simulate the electrosensory signals that result from the JAR behavior.
Surprisingly, the global oscillations appear to enhance directional responses. This result suggests a possible new function of the JAR: to enhance electrosensory processing. The data also support the hypothesis that short-term synaptic depression may have a functional role in the generation of directional responses (Fortune and Rose 2002) and also in the enhancement of those responses by the global oscillations. Because the global synchronous 20- to 50-Hz electrosensory oscillations result in patterns of CNS activity that are similar to gamma-band oscillations seen in a wide variety of neural systems (Bullock and Achimowicz 1994), these data may indicate that gamma-band oscillations modulate short-term synaptic depression which results in enhanced processing of temporal information.
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METHODS |
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; Rose and Call 1993; Rose and Fortune 1996). Intracellular recordings were made in the dorsal 5 layers of the torus of adult Eigenmannia virescens. The method for intracellular recordings was whole cell patch under current clamp as described in Rose and Fortune (1996). Seal resistances were 1–2 G
and resting potentials were –55 to –75 mV. The response properties and mechanisms used in the processing of behaviorally relevant information have been well characterized in the ascending electrosensory systems of these fishes (Heiligenberg 1991; Rose 2004).
For experiments, the electric organ discharge was attenuated (>1,000-fold) and the fish immobilized by intramuscular injection of gallamine triethiodide (Flaxedil; 4 µg/g fish). The fish's electric field was replaced by a sinusoidal mimic, known as the "S1," applied through an electrode in the mouth and an external electrode at the tail (Fig. 1). The frequency of the S1 was adjusted to be within 50 Hz of the animal's natural electric field frequency, and its amplitude was set to 
20 mV/cm near the head. The moving stimulus was presented with combinations of global electrosensory stimuli (see following text). For solitary conditions, a continuous artificial mimic of the fish's own electric field was generated using a wire placed in the mouth and at the tail (Fig. 1B). The global oscillations were produced by adding a second sinusoidal electric field to the tank (Fig. 1, B and C).
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Stimuli
The moving stimulus was a 1.8-cm-wide metal plate with an insulated backing that was moved at a constant velocity parallel to the fish from near the tail to 2 cm past the head and back again at rates between 10 and 20 cm/s (Ramcharitar et al. 2005) (Fig. 1A). Each trial consisted of at least three complete cycles of object motion (i.e., tail to head to tail) (Ramcharitar et al. 2005).
Recordings of responses to the moving stimulus were first obtained with the sinusoidal mimic of the fish's own electric field in the absence of global oscillations. Next, fish were subjected to ongoing, constant frequency (20–50 Hz), global oscillations for a minimum of 1 s prior to initiation of object movement. This duration is known to be sufficient to produce PSPs with stable amplitudes in toral electrosensory neurons (see Fortune and Rose 2000; Rose and Fortune 1999). That is, 1 s of stimulation is sufficient to fully induce the short-term synaptic depression in these neurons.
The global 20- to 50-Hz oscillations were presented using two methods: identical geometry (IG) and differential geometry (DG; Fig. 1, B and C, respectively). In DG, the second field was presented through a pair of electrodes adjacent to or across the fish. DG is a naturalistic method for generating socially derived oscillations as it mimics the orientation of the electric field of a nearby fish. DG, however, results in differences in combined electrical geometry of the field lines compared with the solitary electric field geometry. In IG, the second field was added to the artificial mimic and presented through the electrodes at the head and mouth. The IG stimulation method is not naturalistic but has the advantage that there are no differences in the electric field geometries between solitary and IG stimulation (as shown in Fig. 1B). As a result, any effects of IG stimulation on motion processing are a direct result of the ongoing oscillations.
The range of global stimuli used in this study was defined on the basis of several studies of the physiological properties of toral neurons. Previous studies have demonstrated that both DG and IG can be effective methods to stimulate midbrain electrosensory neurons (Fortune and Rose 1997b, 2000; Rose and Fortune 1999). In many neurons, both IG and DG stimulation can elicit robust, reliable responses; a minority of neurons responds only to DG stimulation (Fortune and Rose 1997b, 2000; Rose and Fortune 1999). For this experiment, we preferentially used IG stimulation. Some neurons were tested with both IG and DG, and others with DG alone. For this study, the stimulation regime that elicited the most reliable and consistent responses from each neuron was used.
We recorded from midbrain neurons that received information from p-type tuberous electroreceptors and ampullary electroreceptors. p-type tuberous electroreceptors encode amplitude modulations of a carrier signal at frequencies within 100 Hz of the fish's own electric field frequency, whereas ampullary electroreceptors detect low-frequency (less than 80 Hz) electric signals (Zakon 1986). As described previously (Fortune and Rose 1997a,b, 2000; Rose and Fortune 1999), global oscillations for tuberous receptors were generated by adding a sinusoidal signal that differed in frequency from the electric field mimic by 20–50 Hz. Global oscillations for ampullary neurons were sinusoids of 20–50 Hz. The JAR produces tuberous but not ampullary oscillations in natural conditions. The p-type tuberous system appears to be an elaboration or duplication of the ampullary system (Fortune and Rose 1997a), and both exhibit identical responses and mechanisms to stimuli with identical temporal frequencies (Ramcharitar et al. 2005).
The specific frequency between 20 and 50 Hz that was used differed between neurons and was chosen on the basis of its frequency response to global stimuli. As has been reported previously, most neurons in the dorsal layers of the torus semicircularis exhibit low- or band-pass responses in the range of 2–50 Hz (Fortune and Rose 1997a). For the global stimulation, we typically used the highest stimulation frequency that elicited visible PSPs in the intracellular recording. This was done for two reasons. First, we were assured that the global stimulus was indeed driving synaptic input during the presentation of the moving object. Second, we measured the magnitude of short-term depression using similar stimuli—if a stimulus did not elicit PSPs, no measurement of short-term depression was possible.
Measurements of physiological data
The magnitudes of PSPs were determined by Fourier analysis of 50- to 750-ms segments of the intracellular responses and by measurements of peak PSP amplitudes (not including spikes) relative to baseline (Fig. 2A). Spikes, when present, were clipped, or, in some cases, low-pass filtering (153-Hz corner frequency) was used before analysis. For Fourier analyses, the peak of the power spectrum (in dB) near the stimulus frequency was used as a measure of the amplitude of stimulus-related PSPs. Measurements of peak PSP amplitudes were converted into dB as the ratio between PSP amplitudes: preferred versus nonpreferred direction for moving stimuli and initial versus steady state for the constant-frequency bursts.
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; Rose and Fortune 1999). One-second-duration, constant stimulus frequency "bursts" were presented: stimulation frequencies were 5, 10, 20, 30, 40, 50 Hz. Bursts of 20 Hz and above can elicit strong PSP depression (Rose and Fortune 1999) that is caused by short-term synaptic depression (Fig. 2, B and C) (Fortune and Rose 2000). The details of these stimulus bursts are identical to the global stimulation used to simulate the addition of a conspecific during the presentation of the moving object, except that they are 1 s in duration and not continuous. This methodology for measuring short-term synaptic depression produces results that correspond to measures of short-term synaptic depression elicited by more traditional paired-pulse stimulation (Fortune and Rose 2000). |
RESULTS |
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were associated with lower resting membrane potentials and smaller PSP amplitudes. Responses to the moving object under solitary electrosensory conditions
Under solitary conditions, the moving object elicited complex PSPs with half-height durations between 55 and 581 ms (Figs. 2 and 3) (Ramcharitar et al. 2005). Peak excitatory responses in each neuron occurred when the object passed along specific areas along the head or trunk of fish. In many neurons, there were additional PSPs, including inhibitory PSPs (IPSPs) adjacent to the largest EPSPs. For this study, we nevertheless focused on measurements of the large EPSPs, as these generated the majority of spiking (which is the ultimate functional output of the neuron that is read by downstream targets) during moving-object stimulation. Responses to the moving object were generally symmetric in shape and timing, but all neurons exhibited some preference for directions of motion (Figs. 3). This preference was measured as differences in PSP amplitudes elicited by the head-to-tail versus tail-to-head stimulation (Fig. 2). Other differences were also seen, including differences in the slopes and durations of PSPs. In 11 neurons the preferred direction was tail to head, and in the opposite direction for 5 neurons. The magnitudes of direction selectivity observed in the solitary condition were between 0.25 and 5.4 dB (mean = 2.49, n = 16; Fig. 4).
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The responses of each neuron to the moving object were also recorded in the presence of ongoing 20- to 50-Hz oscillations. The most dramatic qualitative effects of the addition of the global oscillations were reductions in PSP amplitudes elicited by one direction of object motion (Fig. 3). This reduction in amplitude in the response to one direction of movement results in a greater difference related to the direction of object motion. Indeed, for every neuron in this study, the magnitude of difference in responses to the two directions of object motion was increased with the addition of the global oscillations relative to the solitary conditions (paired t-test, n = 16, P < 0.0001). The magnitudes of direction selectivity in the presence of the global oscillations were between 1.60 and 11.80 dB (mean = 4.88, n = 16; Fig. 4). The magnitude of the change in directional responses associated with the addition of the global oscillations for individual neurons was between 0.18 and 6.4 dB (mean = 2.39, n = 16). We found no qualitative or quantitative differences between the responses to the moving objects in the presence of IG and DG stimulation across neurons.
Relation of short-term synaptic depression to directional responses
The magnitudes of short-term depression observed in this study were between 0.1 and 7.2 dB (mean = 2.79, n = 16), which is similar to previous reports (Fortune and Rose 2000; Rose and Fortune 1999). There was a significant correlation between the magnitude of direction selectivity observed in solitary conditions and the magnitude of short-term synaptic depression (linear regression, R2 = 0.76, P < 0.0001; Fig. 4). Also we observed a significant relation between the magnitude of direction selectivity when the object was presented along with ongoing global 20- to 50-Hz oscillations and the magnitude of short-term synaptic depression (linear regression, R2 = 0.82, P < 0.0001; Fig. 4). Finally, we observed a significant correlation between the magnitude of the enhancement of direction selectivity by the addition of the ongoing global oscillations and short-term synaptic depression (linear regression, R2 = 0.56, P < 0.001).
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DISCUSSION |
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Function of the JAR
The name of the JAR is accurate: the behavior leads to a reduction of the emergent patterns of interference that degrade electrosensory function. Nevertheless, there are alternative solutions to the jamming problem. One solution is to simply move away from conspecifics. Recent data demonstrate that Eigenmannia are preferentially found in aggregates or shoals and as a result are continuously exposed to ongoing global oscillations (Oestreich and Zakon 2005; Tan et al. 2005). Another group, Sternopygus, solves the jamming problem using a sensory processing solution. These animals do not exhibit JAR behaviors and appear to be immune to electrosensory jamming (Bullock et al. 1975; Matsubara and Heiligenberg 1978; Rose and Canfield 1993). This immunity to jamming is conferred by a specialized class of neurons in the electrosensory lateral line lobe (ELL) (Matsubara 1981, 1982).
The JAR requires that fish simultaneously process information from two behaviorally-relevant sources. First, there is information from the global synchronous 20- to 50-Hz (gamma-band) oscillations that are produced by the combination of social behavior and the JAR. Second, there is information from more local, lower frequency stimuli. In a previous study, the magnitudes of midbrain responses to moving local stimuli were dramatically reduced by the addition of lower (<10 Hz) but not by higher-frequency (>15 Hz) global stimuli (Ramcharitar et al. 2005). Here we have shown that the higher-frequency global stimuli have an effect on direction selectivity: direction selectivity is enhanced.
Might the JAR, therefore be a mechanism that has two roles—first to avoid detrimental patterns of interference and, second, to create beneficial patterns of interference. Interestingly, the organization of the ascending electrosensory projections to the midbrain in electric fishes has dynamic features that appear to facilitate the propagation of low-frequency local stimuli and higher-frequency global stimuli like those that result from the JAR. The receptive field properties of neurons in the ELL are dynamic and differ with respect to the spatial extent of the stimulus. Local stimuli tend to elicit low-pass (<10 Hz) or all-pass responses, whereas responses to global stimuli are high-pass (>20 Hz) filtered; descending negative feedback is primarily activated by global stimulation and acts to suppress responses to slow modulations or steady-state levels of signal amplitude (Chacron et al. 2003, 2005; also see Oswald et al. 2004). A function of these dynamic receptive fields may be to allow the same afferent neuron to transmit both the ongoing 20- to 50-Hz global oscillations and lower-frequency local stimuli. In this way, the high-frequency global oscillations elicit short-term synaptic depression at midbrain synapses that may also transmit the local, low-frequency information. The mechanism by which induction of short-term depression may contribute to the enhancement of directional responses in midbrain neurons is not yet known but may be similar to principles described in a model for visual processing of moving images (Chance et al. 1998).
Role of short-term synaptic depression in the generation of direction selectivity
In a model proposed by Chance et al. (1998), short-term synaptic depression limits the rise in PSP amplitude over time, which results in a phase-advance in peak amplitude (Fortune and Rose 2002). For the same pattern of inputs, the peaks of PSPs can be phase shifted by the activation of short-term depression relative to synapses that do not exhibit this depression (see Fortune and Rose 2001, 2002).
Direction selectivity can be achieved by systematic distribution of magnitudes of short-term synaptic depression among afferents with different receptive fields (Chance et al. 1998; Fortune and Rose 2002). Consider two receptive fields at adjacent locations in the receptor array with the same responses to a moving object. Information for one of the receptive fields passes through a synapse with short-term depression and the other does not. If the moving object passes first through the receptive field without depression and shortly thereafter through the receptive field with depression, the peak responses could occur at the same time. This would happen when the phase advance that results from short-term depression is equal to the time disparity between activation of the receptive fields. A neuron receiving these simultaneous inputs from the two receptive fields could respond strongly to the moving object. Movement in the opposite direction would reverse the order of stimulation of receptive fields. As a result, the peak responses would occur at different times. A neuron that received information from these two receptive fields would potentially not respond (Fortune and Rose 2002). This model can produce direction selectivity in circuits that use only excitatory synapses or in circuits that use a combination of excitatory and inhibitory synapses (Fortune and Rose 2002).
In this same manner, directionality could be further enhanced if information from one receptive field passed through a facilitating synapse, such that the response peak was delayed (Fortune and Rose 2001, 2002). Neurons in the torus can exhibit both short-term synaptic depression and facilitation (Fortune and Rose 2000). The depression and facilitation are differentially activated in such neurons: high-temporal frequency stimuli, like post-JAR global oscillations, maximally elicit depression and not facilitation, whereas low-temporal frequency stimuli can strongly drive facilitation.
The hypothesis that short-term synaptic plasticity is used as a form of delay line is difficult to test in intact systems. The pattern of afferent activity from moving stimuli will necessarily activate the synaptic plasticity and as a result, the plasticity and other mechanisms for processing of motion-related activity cannot be easily disassociated. Also, because the model requires the convergence of information through synapses that exhibit plasticity and others that do not, it is unclear what sort of measurements of depression one might expect from direct afferent stimulation. Nevertheless, the electrosensory midbrain contains the processing units required by the model. First, neurons in the torus exhibit dramatic differences in the magnitude of short-term synaptic depression that are elicited by sensory stimuli and direct, paired-pulse stimulation of afferents (Fortune and Rose 2000). Second, moving stimuli elicit reliable responses in these neurons, and many neurons exhibit strongly directional responses.
What intrigued us initially was the possibility that we could use naturally occurring electrosensory stimuli in Eigenmannia to modulate the strength of short-term synaptic plasticity in the midbrain. If short-term synaptic depression has a role in the generation of directional responses, then the modulation of short-term plasticity by these stimuli should dramatically alter directionality. Specifically, if short-term synaptic depression is used as a form of delay line, alteration of the depression by the addition of the global stimulus should result in changes in the delays that result from depression and thus potentially degrade the directional responses. Indeed we expected that modulation of short-term plasticity by the addition of broad-field electrosensory stimulus would lead to a dramatic degradation of direction selectivity.
Remarkably, the opposite result occurred: the addition of the depressing broad-field stimulus led to an increase in direction selectivity. There are many possible substrates for this unexpected phenomenon. The most likely candidate at present is short-term synaptic plasticity, which is supported by our observation of a strong correlation between the magnitude of the enhancement of directionality and the magnitude of short-term depression. Such a mechanism might include the modulation of excitatory and inhibitory synapses (Fortune and Rose 2002). Other mechanisms are possible, however, and include short-term synaptic facilitation, descending inputs to the ELL (Bratton and Bastian 1990), and nonclassical receptive field properties in the ELL (Chacron et al. 2003), some form of gain modulation (Chance et al. 2002), among others.
Of particular interest are mechanisms present in the afferent system, the ELL, that may also contribute to the complex direction selectivity observed in toral neurons. The ELL receives descending inputs from the nucleus praeeminentialis (NPd) that enhance responses of ELL neurons to local stimuli such as prey (Bratton and Bastian 1990). These descending inputs must be delayed relative to incoming inputs and therefore may produce focal temporal disparities for motion processing. Other ELL mechanisms may also result in nonlinearities in the responses to moving objects including voltage-dependent EPSPs, dendritic Na+ conductances, and nonlinearities associated with bursts (Berman et al. 1997).
Interestingly, the temporal filtering properties of ELL neurons in Apteronotus differ in relation to the spatial organization of the stimulus: ELL neurons exhibit high-pass responses to broad-field stimuli and low-pass responses to local stimuli (Chacron et al. 2003). The mechanisms for this spatially dependent change appear to result from descending feedback and differ among the classes of ELL pyramidal cells (Chacron et al. 2005). Although not tested, this circuitry likely results in nonlinear interactions during concomitant presentation of local and global stimuli. Analyses of data from concomitant presentation of beats and chirps, both of which are global signals, demonstrated an interaction at the level of the receptor afferents that resulted from spike frequency adaptation (Benda et al. 2005). Finally, responses to moving objects in the presence of beat frequencies of 32 Hz in Apteronotus leptorhynchus are robust (Bratton and Bastian 1990) despite the fact that ELL neurons respond more strongly to higher AM rates (Bastian 1987) and may exhibit some directionality in the responses (see Fig. 5 of Bratton and Bastian 1990).
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Mammalian cortical systems commonly produce oscillations in a range of frequencies centered around 40 Hz (Csibra et al. 2000): these intrinsic cortical oscillations are known as gamma-band oscillations. Further, gamma-band oscillations appear to be generated during the processing of behaviorally-relevant, time-varying information in a phylogenetically diverse array of vertebrate species (Bullock and Achimowicz 1994). The functional role of gamma-band oscillations is a subject of great speculation.
Most species generate gamma-band oscillations using intrinsic mechanisms. Intrinsic gamma-band oscillations emerge at many levels in the nervous system among species (e.g., Csibra et al. 2000; Ishikane et al. 2005; Lutzenberger et al. 2002; Neiman and Russell 2004). In Apteronotus, a closely related species of electric fish, certain electrosensory stimuli can induce intrinsic oscillations in the gamma range using central mechanisms (Doiron et al. 2003). Eigenmannia appear to be unusual in that these animals generate gamma-band oscillations in CNS circuits using an external source: via electrosensory signals that result from social behavior and the JAR.
Previous work has shown that there is a linkage between sensory-driven gamma-band oscillations and short-term synaptic depression in Eigenmannia (Fortune and Rose 2000). The sensory-driven gamma-band oscillations may therefore function to modulate synaptic weights for the purpose of enhancing the temporal processing of streams of information (Lutzenberger et al. 2002). The critical observation is that identical stimuli presented alone or simultaneously with a gamma-band oscillation can result in dramatic differences in stimulus-related information processing in the brain (Fig. 5). The specific mechanisms by which these changes in information processing lead to enhancement of temporal features remain unclear. Nevertheless, the key feature of this model is that the effect of global synchronous gamma-band spiking activity is measured by its affect on the processing of simultaneously occurring streams of information in single neurons.
This interaction between gamma-band oscillations and single neuron processing by the modulation of short-term synaptic plasticity may be a general mechanism for the enhancement of temporal processing in vertebrates. Short-term synaptic plasticity is ubiquitous in sensory systems of vertebrates (Abbott and Regehr 2004; Fortune and Rose 2001). The induction of global synchronous gamma-band oscillations associated with attention (Shibata et al. 1999), for example, may be used to enhance temporal processing of information from a specific region of the sensory array. Similarly, gamma-band oscillations associated with voluntary movements (Donoghue et al. 1998) may enhance the temporal processing of sensory feedback generated during motor behavior. These ideas can be tested in weakly electric fish using psychophysical tests under solitary and post-JAR social conditions.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: E. S. Fortune, Dept. of Psychological and Brain Sciences, 3400 N. Charles St., Baltimore, MD 21218 (E-mail: eric.fortune{at}jhu.edu)
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, movement of the object stimulus starting at the tail, moving beyond the head, and traveling back toward the tail. Measurements were made after the spikes were removed by clipping or low-pass filtering. 
, excitatory postsynaptic potentials (EPSPSs) measured for direction selectivity. In this case, the responses for the head- to-tail and tail-to-head directions of object movement were similar. B and C: examples of responses to a 1-s-duration 20-Hz AM (bottom). 
) and with global 20- to 50-Hz oscillations (
, each above the corresponding filled dot from the same neuron). There is a statistically significant positive correlation between short-term depression and the direction selectivity in both conditions (regression lines).