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G S Pollack

Publications and source records attributed to G S Pollack.

18 recordsLinked to original sources

Differential temporal coding of rhythmically diverse acoustic signals by a single interneuron.

The omega neuron 1 (ON1) of the cricket Teleogryllus oceanicus responds to conspecific signals (4.5 kHz) and to the ultrasonic echolocation sounds used by hunting, insectivorous bats. These signals differ in temporal structure as well as in carrier frequency. We show that ON1's temporal coding properties vary with carrier frequency, allowing it to encode both of these behaviorally important signals. Information-transfer functions show that coding of 4.5 kHz is limited to the range of amplitude-modulation components that occur in cricket songs (<32 Hz), whereas coding of 30-kHz stimuli extends to the higher pulse rates that occur in bat sounds ( approximately 100 Hz). Nonlinear coding contributes to the information content of ON1's spike train, particularly for 30-kHz stimuli with high intensities and large modulation depths. Phase locking to sinusoidal amplitude envelopes also extends to higher AM frequencies for ultrasound stimuli. ON1s frequency-specific behavior cannot be ascribed to differences in the shapes of information-transfer functions of low- and high-frequency-tuned receptor neurons, both of which are tuned more broadly to AM frequencies than ON1. Coding properties are nearly unaffected by contralateral deafferentation. ON1's role in auditory processing is to increase binaural contrast through contralateral inhibition. We hypothesize that its frequency-specific temporal coding properties optimize binaural contrast for sounds with both the spectral and temporal features of behaviorally relevant signals.

Acoustic Stimulation↗

Sensory cues for sound localization in the cricket Teleogryllus oceanicus: interaural difference in response strength versus interaural latency difference.

Two potential sensory cues for sound location are interaural difference in response strength (firing rate and/or spike count) and in response latency of auditory receptor neurons. Previous experiments showed that these two cues are affected differently by intense prior stimulation; the difference in response strength declines and may even reverse in sign, but the difference in latency is unaffected. Here, I use an intense, constant tone to disrupt localization cues generated by a subsequent train of sound pulses. Recordings from the auditory nerve confirm that tone stimulation reduces, and sometimes reverses, the interaural difference in response strength to subsequent sound pulses, but that it enhances the interaural latency difference. If sound location is determined mainly from latency comparison, then behavioral responses to a pulse train following tone stimulation should be normal, but if the main cue for sound location is interaural difference in response strength, then post-tone behavioral responses should sometimes be misdirected. Initial phonotactic responses to the post-tone pulse train were frequently directed away from, rather than towards, the sound source, indicating that the dominant sensory cue for sound location is interaural difference in response strength.

Acoustic Stimulation↗

Analysis of temporal patterns of communication signals.

Temporal pattern is a crucial feature of communication signals, and neurons in the brains of many animals respond selectively to behaviorally relevant temporal features of sensory stimuli. Many aspects of neural function contribute to this selectivity, including membrane biophysics, channel properties, synaptic physiology and network structure.

Animal Communication↗

Neural representation of sound amplitude by functionally different auditory receptors in crickets.

The physiological characteristics of auditory receptor fibers (ARFs) of crickets, a model system for studying auditory behaviors and their neural mechanisms, are investigated. Unlike auditory receptor neurons of many animals, cricket ARFs fall into three distinct populations based on characteristic frequency (CF) [Imaizumi and Pollack, J. Neurosci. 19, 1508-1516 (1999)]. Two of these have CFs similar to the frequency component of communication signals or of ultrasound produced by predators, and a third population has intermediate CF. Here, sound-amplitude coding by ARFs is examined to gain insights to how behaviorally relevant sounds are encoded by populations of receptor neurons. ARFs involved in acoustic communication comprise two distinct anatomical types, which also differ in physiological parameters (threshold, response slope, dynamic range, minimum latency, and sharpness of tuning). Thus, based on CF and anatomy, ARFs comprise four populations. Physiological parameters are diverse, but within each population they are systematically related to threshold. The details of these relationships differ among the four populations. These findings open the possibility that different ARF populations differ in functional organization.

Animals↗

Mechanisms of frequency-specific responses of omega neuron 1 in crickets (Teleogryllus oceanicus): a polysynaptic pathway for song?

In crickets (Teleogryllus oceanicus), the auditory interneuron omega neuron 1 (ON1) responds to sounds over a wide range of frequencies but is most sensitive to the frequency of conspecific songs (4.5 kHz). Response latency is longest for this same frequency. We investigate the mechanisms that might account for the longer latency of ON1 to cricket-like sounds. Intracellular recordings revealed no evidence for appropriately timed postsynaptic inhibition of ON1 that might increase its latency, nor was latency affected by picrotoxin. The onset of excitatory postsynaptic potentials (EPSPs) was delayed for 4.5 kHz stimuli compared with ultrasound stimuli, pointing to a presynaptic locus for the latency difference. When ON1 is stimulated with high frequencies, discrete, apparently unitary EPSPs can be recorded in its dendrite, and these are latency-locked to spikes recorded simultaneously in the auditory nerve. This suggests that input to ON1 from high-frequency-tuned auditory receptor neurons is monosynaptic. In agreement with this, brief ultrasound stimuli evoke a single, short-latency EPSP in ON1. In contrast, the EPSP evoked by a brief 4.5 kHz stimulus consists of an early component, similar in latency to that evoked by ultrasound and possibly evoked by ultrasound-tuned receptors, and a later, dominant component. We interpret the early peak as arising from a monosynaptic afferent pathway and the late peak from a polysynaptic afferent pathway. Multiple-peak EPSPs, with timing similar to those evoked by sound stimuli, were also evoked by electrical stimulation of the auditory nerve.

Acoustic Stimulation↗

Effects of inhibitory timing on contrast enhancement in auditory circuits in crickets (Teleogryllus oceanicus).

In crickets (Teleogryllus oceanicus), the paired auditory interneuron Omega Neuron 1 (ON1) responds to sounds with frequencies in the range from 3 to 40 kHz. The neuron is tuned to frequencies similar to that of conspecific songs (4.5 kHz), but its latency is longest for these same frequencies by a margin of 5-10 ms. Each ON1 is strongly excited by input from the ipsilateral ear and inhibits contralateral auditory neurons that are excited by the contralateral ear, including the interneurons ascending neurons 1 and 2 (AN1 and AN2). We investigated the functional consequences of ON1's long latency to cricket-like sound and the resulting delay in inhibition of AN1 and AN2. Using dichotic stimuli, we controlled the timing of contralateral inhibition of the ANs relative to their excitation by ipsilateral stimuli. Advancing the stimulus to the ear driving ON1 relative to that driving the ANs "subtracted" ON1's additional latency to 4.5 kHz. This had little effect on the spike counts of AN1 and AN2. The response latencies of these neurons, however, increased markedly. This is because in the absence of a delay in ON1's response, inhibition arrived at AN1 and AN2 early enough to abolish the first spikes in their responses. This also increased the variability of AN1 latency. This suggests that one possible function of the delay in ON1's response may be to protect the precise timing of the onset of response in the contralateral AN1, thus preserving interaural difference in response latency as a reliable potential cue for sound localization. Hyperpolarizing ON1 removed all detectable contralateral inhibition of AN1 and AN2, suggesting that ON1 is the main, if not the only, source of contralateral inhibition.

Acoustic Stimulation↗

Sensory habituation of auditory receptor neurons: implications for sound localization.

Auditory receptor neurons exhibit sensory habituation; their responses decline with repeated stimulation. We studied the effects of sensory habituation on the neural encoding of sound localization cues using crickets as a model system. In crickets, Teleogryllus oceanicus, sound localization is based on binaural comparison of stimulus intensity. There are two potential codes at the receptor-neuron level for interaural intensity difference: interaural difference in response strength, i.e. spike rate and/or count, and interaural difference in response latency. These are affected differently by sensory habituation. When crickets are stimulated with cricket-song-like trains of sound pulses, response strength declines for successive pulses in the train, and the decrease becomes more pronounced as the stimulus intensity increases. Response decrement is thus greater for receptors serving the ear ipsilateral to the sound source, where intensity is higher, resulting in a decrease in the interaural difference in response strength. Sensory habituation also affects response latency, which increases for responses to successive sound pulses in the stimulus train. The change in latency is independent of intensity, and thus is similar for receptors serving both ears. As a result, interaural latency difference is unaffected by sensory habituation and may be a more reliable cue for sound localization.

Acoustic Stimulation↗

Neural coding of sound frequency by cricket auditory receptors.

Crickets provide a useful model to study neural processing of sound frequency. Sound frequency is one parameter that crickets use to discriminate between conspecific signals and sounds made by predators, yet little is known about how frequency is represented at the level of auditory receptors. In this paper, we study the physiological properties of auditory receptor fibers (ARFs) by making single-unit recordings in the cricket Teleogryllus oceanicus. Characteristic frequencies (CFs) of ARFs are distributed discontinuously throughout the range of frequencies that we investigated (2-40 kHz) and appear to be clustered around three frequency ranges (</=5.5, 10-12, and >/=18 kHz). A striking characteristic of cricket ARFs is the occurrence of additional sensitivity peaks at frequencies other than CFs. These additional sensitivity peaks allow crickets to detect sound over a wide frequency range, although the CFs of ARFs cover only the frequency bands mentioned above. To the best of our knowledge, this is the first example of the extension of an animal's hearing range through multiple sensitivity peaks of auditory receptors.

Animals↗

Taste sensilla of flies: function, central neuronal projections, and development.

Taste sensilla of flies are composed of only a few cells, all of which have different functions. Depending on the species and on the sensillum type, there are from 2-5 neurons, each of which has its own stimulus specificity, and each of which makes a different contribution to the fly's behavior. In addition, taste sensilla include several nonneuronal cells that are important both for the development of the sensillum and for its functioning. The component cells of a sensillum derive from a single epidermal precursor according to a stereotyped sequence of mitoses. This review focuses on the different phenotypes of the component cells of taste sensilla, particularly the stimulus sensitivity and central neuronal anatomy of the receptor neurons, and on the development of this multicellular organ from a single precursor cell.

Animals↗

SWEEPS: a program for the acquisition and analysis of neurophysiological data.

I describe SWEEPS, a program for the acquisition and analysis of neurophysiological data written with LabWindows/CVI. SWEEPS includes many features of general interest to neurobiologists, such as digital filtering, window discrimination, and the construction of peristimulus time histograms. As the program is written using LabWindows/CVI, a C-programming system which includes routines for many data-processing and display tasks, it can be easily modified to accommodate new analysis needs as they arise.

Animals↗

Birth times of neurons in labellar taste sensilla of the blowfly Phormia regina.

We studied the birth times of neurons of labellar taste sensilla in blowflies using incorporation of the thymidine analogue 5-bromodeoxyuridine (BrdU) as an indicator of birth time. We found that one of the two main sensillum types, the taste papillae, arise according to a clear spatial gradient of birth times, whereas the other sensillum type, taste hairs, arise without any apparent spatial ordering. Within each sensillum type, there was a strong tendency for either all or none of the neurons to have incorporated BrdU. Among those rare sensilla in which only some of the neurons incorporated BrdU, there were clear patterns of the distribution of labeled and unlabeled neurons per sensillum. These results suggest that subsets of the neurons of a sensillum are siblings, and thus argue against the possibility that the several neurons of a sensillum arise from a single stem cell precursor through repeated asymmetrical divisions.

Aging↗

From embryo to adult: anatomy and development of a leg sensory organ in Phormia regina Meigen (Insecta: Diptera). I. Anatomy and physiology of a larval "leg" sensory organ.

Neurons within the precursor of the adult leg, the imaginal disc, innervate a larval sense organ, Keilin's organ. Electron microscopical investigations of first instar larvae show that five dendrites end at the organ: three insert at the bases of the three hairs of the organ and two end against the cuticle, without any apparent cuticular specialization. In third instar larvae, the imaginal leg discs invaginate into the body cavity, and only four of the dendrites (the outer segments of which become greatly elongated) remain in contact with Keilin's organ. The axons of the neurons that supply Keilin's organ project into a ventral neuropile region of the central nervous system, with a pattern that resembles the projections of other larval sensilla. Electrical activity can be recorded from neurons of the imaginal disc in response to mechanical stimulation.

Afferent Pathways↗

From embryo to adult: anatomy and development of a leg sensory organ in Phormia regina, Meigen (Insecta: Diptera). II. Development and persistence of sensory neurons.

The imaginal leg disc of Phormia regina contains eight neurons that arise during embryogenesis. Five of the neurons are associated with Keilin's organ, and of these five, two persist to the adult fly. Two new neurons arise at about the time of pupariation and flank each of these persisting neurons, forming two triplets of cells. Both triplets can be followed throughout metamorphosis; in the late pupa they are situated anteriorly and posteriorly at the tip of the fifth tarsomere. Two triplets of cuticular specializations are found at corresponding positions in the adult fly, each consisting of two campaniform sensilla and a trichoid hair. The central member of each set of sensilla, a campaniform sensillum, is associated with the persisting cell.

Animals↗

The development of the sensory organs of the legs in the blowfly, Phormia regina.

The development of the sensory neurons of the legs of the blowfly, Phormia regina has been described from the third instar larva to the late pupa using immunohistochemical staining. The leg discs of the third instar larva contain 8 neurons of which 5 come to lie in the fifth tarsomere of the developing leg. Whereas 2 neurons persist at least to the late pupa, the other cells degenerate. The first neurons of gustatory sensilla arise in the fifth tarsomere at about 1.5 h after formation of the puparium. Most of these sensilla, however, appear within a short time period beginning at about 18 h. The femoral chordotonal sensory neurons first appear at the time of formation of the puparium, as a mass of cells situated in the distal femur. During later pupal development 2 groups of these cells come to lie at the femur-trochanter border, where they become the proximal femoral chordotonal organ of the adult; the remaining cells become the distal femoral chordotonal organ. Other scolopidial neurons appear later in development. The nerve pathways of the late pupal leg are established either by the axons of the cells that are present in the larval leg disc or by new outgrowing processes of sensory neurons. In the tibia, the initial direction of new outgrowth differs in different regions of the segment: proximal tibial neurons grow distally, while distal tibial neurons grow initially proximally.

Animals↗

Selective attention in an insect auditory neuron.

Previous work (Pollack, 1986) showed that an identified auditory neuron of crickets, the omega neuron, selectively encodes the temporal structure of an ipsilateral sound stimulus when a contralateral stimulus is presented simultaneously, even though the contralateral stimulus is clearly encoded when it is presented alone. The present paper investigates the physiological basis for this selective response. The selectivity for the ipsilateral stimulus is a result of the apparent intensity difference of ipsi- and contralateral stimuli, which is imposed by auditory directionality; when simultaneous presentation of stimuli from the 2 sides is mimicked by presenting low- and high-intensity stimuli simultaneously from the ipsilateral side, the neuron responds selectively to the high-intensity stimulus, even though the low-intensity stimulus is effective when it is presented alone. The selective encoding of the more intense (= ipsilateral) stimulus is due to intensity-dependent inhibition, which is superimposed on the cell's excitatory response to sound. Because of the inhibition, the stimulus with lower intensity (i.e., the contralateral stimulus) is rendered subthreshold, while the stimulus with higher intensity (the ipsilateral stimulus) remains above threshold. Consequently, the temporal structure of the low-intensity stimulus is filtered out of the neuron's spike train. The source of the inhibition is not known. It is not a consequence of activation of the omega neuron. Its characteristics are not consistent with those of known inhibitory inputs to the omega neuron.

Acoustic Stimulation↗

Correlations between structure, topographic arrangement, and spectral sensitivity of sound-sensitive interneurons in crickets.

The morphology of nine prothoracic, sound-activated, interganglionic interneurons in Teleogryllus oceanicus is described. Only two of the neurons can, on anatomical grounds, receive input directly from auditory receptors. The morphology of many of the cells suggests that they may provide output to motor areas. The nine cells can be divided into two groups on the basis of their spectral sensitivity: high-frequency neurons and low-frequency neurons. Correlations were found between morphology and spectral sensitivity. High-frequency neurons have a ventromedial soma, dorsally positioned neuropile processes, and an axon in the lateral half of the promesothoracic connective. In contrast, low-frequency neurons have a dorsal and/or laterally positioned soma, neuropile processes in the ventral portion of the prothoracic ganglion, and an axon projecting in the medial half of the connective. These findings reveal the existence of a crude tonotopic organization of central neurons. In addition, they provide hints as to the type of output and the targets of these neurons.

Animals↗

Age-dependent occurrence of an ascending axon on the omega neuron of the cricket, Teleogryllus oceanicus.

The omega neurons (ON1s) are a mirror-symmetrical pair of identified prothoracic auditory interneurons of crickets which have been previously described as intraganglionic. Using intracellular techniques we stained ON1s of female Teleogryllus oceanicus and found that many ON1s have axons which project anteriorly out of the prothoracic ganglion. The ascending axon arises contralateral to the soma at the most anteriolateral bend of the bow-shaped process of an otherwise "archetypical" ON1 and travels up the neck connective in a ventral position just inside the connective tissue sheath. The occurrence of the ascending axon is age-dependent. Seventy-five percent of ON1s stained in late nymphal stages and in young adults had an ascending axon while only 30% of ON1s in older adults had an ascending axon. Evidence is presented to show that ON1s having ascending axons are developmental variants of the "archetypical" ON1 and do not represent a separate neuron type. The two morphological types of ON1s are not distinguishable on the basis of their responses to sound stimuli having carrier frequencies of 3.5-60 kHz. Although we know that the ascending axon conducts action potentials, its target and terminal morphology are not yet known.

Age Factors↗

Steering responses of flying crickets to sound and ultrasound: Mate attraction and predator avoidance.

We investigated the steering responses of tethered, flying adult female crickets (Teleogryllus oceanicus) to acoustic stimulation. Crickets responded directionally to directional sound stimulation by bending their abdomens and hind legs to one side. We interpret this response as an attempt to turn. When stimulated with a model of conspecific calling song with a carrier frequency of from 3 to 9 kHz, crickets turned toward the sound source. We believe that this indicates a positive phonotactic response of flying females to calling, conspecific males. When offered a choice between conspecific song and the song of another species, females turned exclusively toward conspecific song, demonstrating that the response is species specific. The direction of the response is dependent on the carrier frequency of the song, and it demonstrates frequency discrimination. Females turned toward calling song when it was played at carrier frequencies from 3 to 9 kHz, but they turned away from the same song pattern played at carrier frequencies from 30 to 70 kHz. This negative phonotaxis to ultrasonic stimuli suggests that crickets, like some other nocturnal flying insects, can evade bats by acoustic detection.

Journal Article↗