Distribution of response types across entire hemispheres of the mustached bat's auditory cortex

Fitzpatrick, Douglas C.; Suga, Nobuo; Olsen, John

doi:10.1002/(sici)1096-9861(19980216)391:1<353::aid-cne13>3.0.co;2-t

Cited by 22 publications

(25 citation statements)

References 66 publications

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“…In the mustached bat, Pteronotus parnellii , social calls associated with aggressive interactions trigger transient as well as persistent activity within neurons in the basoloateral amygdala (Naumann and Kanwal, 2007, 2011; Peterson and Wenstrup, 2012). This is consistent with the presence of anterograde labeling in this region of the amygdala after injection of tracers into physiologically identified areas of the auditory cortex in mustached bats (Fitzpatrick et al, 1998). It is generally understood that sensory information flows from the lateral amygdala (LA) to the basal and central amygdala (BA and CA, respectively), although short paths from the LA to the CA, bypassing the BA, and reciprocal connections between these and other nuclei also exist (Pitkanen et al, 1997).…”

Section: Introductionsupporting

confidence: 80%

Stimulation of the basal and central amygdala in the mustached bat triggers echolocation and agonistic vocalizations within multimodal output

2014

Front. Physiol.

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The neural substrate for the perception of vocalizations is relatively well described, but how their timing and specificity are tightly coupled with accompanying physiological changes and context-appropriate behaviors remains unresolved. We hypothesized that temporally integrated vocal and emotive responses, especially the expression of fear, vigilance and aggression, originate within the amygdala. To test this hypothesis, we performed electrical microstimulation at 461 highly restricted loci within the basal and central amygdala in awake mustached bats. At a subset of these sites, high frequency stimulation with weak constant current pulses presented at near-threshold levels triggered vocalization of either echolocation pulses or social calls. At the vast majority of locations, microstimulation produced a constellation of changes in autonomic and somatomotor outputs. These changes included widespread co-activation of significant tachycardia and hyperventilation and/or rhythmic ear pinna movements (PMs). In a few locations, responses were constrained to vocalization and/or PMs despite increases in the intensity of stimulation. The probability of eliciting echolocation pulses vs. social calls decreased in a medial-posterior to anterolateral direction within the centrobasal amygdala. Microinjections of kainic acid (KA) at stimulation sites confirmed the contribution of cellular activity rather than fibers-of-passage in the control of multimodal outputs. The results suggest that localized clusters of neurons may simultaneously modulate the activity of multiple central pattern generators (CPGs) present within the brainstem.

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Section: Introductionsupporting

confidence: 80%

Stimulation of the basal and central amygdala in the mustached bat triggers echolocation and agonistic vocalizations within multimodal output

2014

Front. Physiol.

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“…Facilitative combination-sensitive responses are abundant in several areas of the mustached bat's auditory cortex (Suga and O'Neill, 1979; Suga et al, 1983; Suga and Horikawa, 1986; Edamatsu et al, 1989; Fitzpatrick et al, 1998) and thalamus (Olsen and Suga, 1991a,b; Wenstrup and Grose, 1995; Yan and Suga, 1996a; Wenstrup, 1999). In IC, these facilitative responses are commonly observed in frequency representations above 30 kHz (Mittmann and Wenstrup, 1995; Portfors and Wenstrup, 1999; Leroy and Wenstrup, 2000).…”

Section: Mechanisms Underlying Combination-sensitive Facilitationmentioning

confidence: 99%

Mechanisms of spectral and temporal integration in the mustached bat inferior colliculus

Wenstrup¹,

Nataraj²,

Sanchez³

2012

Front. Neural Circuits

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This review describes mechanisms and circuitry underlying combination-sensitive response properties in the auditory brainstem and midbrain. Combination-sensitive neurons, performing a type of auditory spectro-temporal integration, respond to specific, properly timed combinations of spectral elements in vocal signals and other acoustic stimuli. While these neurons are known to occur in the auditory forebrain of many vertebrate species, the work described here establishes their origin in the auditory brainstem and midbrain. Focusing on the mustached bat, we review several major findings: (1) Combination-sensitive responses involve facilitatory interactions, inhibitory interactions, or both when activated by distinct spectral elements in complex sounds. (2) Combination-sensitive responses are created in distinct stages: inhibition arises mainly in lateral lemniscal nuclei of the auditory brainstem, while facilitation arises in the inferior colliculus (IC) of the midbrain. (3) Spectral integration underlying combination-sensitive responses requires a low-frequency input tuned well below a neuron's characteristic frequency (ChF). Low-ChF neurons in the auditory brainstem project to high-ChF regions in brainstem or IC to create combination sensitivity. (4) At their sites of origin, both facilitatory and inhibitory combination-sensitive interactions depend on glycinergic inputs and are eliminated by glycine receptor blockade. Surprisingly, facilitatory interactions in IC depend almost exclusively on glycinergic inputs and are largely independent of glutamatergic and GABAergic inputs. (5) The medial nucleus of the trapezoid body (MNTB), the lateral lemniscal nuclei, and the IC play critical roles in creating combination-sensitive responses. We propose that these mechanisms, based on work in the mustached bat, apply to a broad range of mammals and other vertebrates that depend on temporally sensitive integration of information across the audible spectrum.

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“…The neural comparisons facilitate the analysis of spectrally and temporally complex vocalizations. Although these properties occur in the forebrains of many vertebrates, from frogs to birds to primates (Fuzessery and Feng 1983;Margoliash and Fortune 1992;Rauschecker 1997), their physiological and organizational features have been described best in the mustached bat (Fitzpatrick et al 1998b;Ohlemiller et al 1996;O'Neill and Suga 1982;Suga et al 1983). The focus of this paper is on physiological and organizational properties in the medial geniculate body (MGB) that may contribute to this specialized auditory cortex.…”

Section: Introductionmentioning

confidence: 99%

“…1) to extract information about a target's distance and movement. The mapping of sonar-related response properties across subregions of auditory cortex represents one of the most extensive studies of behaviorally relevant functional organization in mammalian auditory cortex (Fitzpatrick et al 1998b;O'Neill and Suga 1982;Suga and O'Neill 1979;Suga et al 1983). The mustached bat's highly developed acoustic communication (Kanwal et al 1994) also uses combination-sensitive responses.…”

Section: Introductionmentioning

confidence: 99%

“…1). In auditory cortex, neurons sensitive to combinations of FM signals display physiological properties and organization that are not shared by neurons tuned to the constant frequency (CF) component in sonar signals or by neurons tuned to frequencies outside the sonar bands (Fitzpatrick et al 1998b;Suga et al 1983). One physiological property of the neurons responding to FM bands is delay…”

Section: Introductionmentioning

confidence: 99%

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Frequency Organization and Responses to Complex Sounds in the Medial Geniculate Body of the Mustached Bat

Wenstrup

1999

Journal of Neurophysiology

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The auditory cortex of the mustached bat (Pteronotus parnellii) displays some of the most highly developed physiological and organizational features described in mammalian auditory cortex. This study examines response properties and organization in the medial geniculate body (MGB) that may contribute to these features of auditory cortex. About 25% of 427 auditory responses had simple frequency tuning with single excitatory tuning curves. The remainder displayed more complex frequency tuning using two-tone or noise stimuli. Most of these were combination-sensitive, responsive to combinations of different frequency bands within sonar or social vocalizations. They included FM-FM neurons, responsive to different harmonic elements of the frequency modulated (FM) sweep in the sonar signal, and H1-CF neurons, responsive to combinations of the bat's first sonar harmonic (H1) and a higher harmonic of the constant frequency (CF) sonar signal. Most combination-sensitive neurons (86%) showed facilitatory interactions. Neurons tuned to frequencies outside the biosonar range also displayed combination-sensitive responses, perhaps related to analyses of social vocalizations. Complex spectral responses were distributed throughout dorsal and ventral divisions of the MGB, forming a major feature of this bat's analysis of complex sounds. The auditory sector of the thalamic reticular nucleus also was dominated by complex spectral responses to sounds. The ventral division was organized tonotopically, based on best frequencies of singly tuned neurons and higher best frequencies of combination-sensitive neurons. Best frequencies were lowest ventrolaterally, increasing dorsally and then ventromedially. However, representations of frequencies associated with higher harmonics of the FM sonar signal were reduced greatly. Frequency organization in the dorsal division was not tonotopic; within the middle one-third of MGB, combination-sensitive responses to second and third harmonic CF sonar signals (60-63 and 90-94 kHz) occurred in adjacent regions. In the rostral one-third, combination-sensitive responses to second, third, and fourth harmonic FM frequency bands predominated. These FM-FM neurons, thought to be selective for delay between an emitted pulse and echo, showed some organization of delay selectivity. The organization of frequency sensitivity in the MGB suggests a major rewiring of the output of the central nucleus of the inferior colliculus, by which collicular neurons tuned to the bat's FM sonar signals mostly project to the dorsal, not the ventral, division. Because physiological differences between collicular and MGB neurons are minor, a major role of the tecto-thalamic projection in the mustached bat may be the reorganization of responses to provide for cortical representations of sonar target features.

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Distribution of response types across entire hemispheres of the mustached bat's auditory cortex

Cited by 22 publications

References 66 publications

Stimulation of the basal and central amygdala in the mustached bat triggers echolocation and agonistic vocalizations within multimodal output

Stimulation of the basal and central amygdala in the mustached bat triggers echolocation and agonistic vocalizations within multimodal output

Mechanisms of spectral and temporal integration in the mustached bat inferior colliculus

Frequency Organization and Responses to Complex Sounds in the Medial Geniculate Body of the Mustached Bat

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