Functional Mapping of the Auditory Midbrain during Mate Call Reception

Hoke, Kim L.; Burmeister, Sabrina S.; Fernald, Russell D.; Rand, A. Stanley; Ryan, Michael J.; Wilczynski, Walter

doi:10.1523/jneurosci.2079-04.2004

Cited by 81 publications

(93 citation statements)

References 53 publications

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“…In addition, the increase in firing rate continued past the stimulus presentation leading to the conclusion that acoustic stimulation acts as a modulator of ongoing activity within central endocrine control areas (Allison, 1992). Although neurophysiological work has not been done in túngara frogs, Hoke et al (2004Hoke et al ( , 2005 demonstrated midbrain activation and hypothalamic sensitivity to conspecific calls in this species using immediate early gene activation. Increases in neural activity within the central endocrine regions translate into elevated gonadal steroid concentrations in male anurans (Burmeister and Wilczynski, 2000;Chu and Wilczynski, 2001).…”

Section: Discussionmentioning

confidence: 99%

Social regulation of plasma estradiol concentration in a female anuran

Lynch

Wilczynski

2006

Hormones and Behavior

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The behavior of an individual within a social aggregation profoundly influences behavior and physiology of other animals within the aggregation in such a way that these social interactions can enhance reproductive success, survival and fitness. This phenomenon is particularly important during the breeding season when males and female must synchronize their reproductive efforts. We examined whether exposure to conspecific social cues can elevate sex steroid levels, specifically estradiol and androgens, in female túngara frogs (Physalaemus pustulosus). We compared plasma estradiol and androgen concentrations in wild-caught females before and after exposure to either natural mate choruses or random tones. After exposure to mate choruses for 10 consecutive nights, estradiol concentrations were significantly elevated whereas there was no significant elevation in estradiol concentrations in the group of females exposed to random tones for 10 nights. Plasma androgen concentrations were not significantly changed after exposure to either natural mate choruses or random tones for 10 consecutive nights. Social modulation of estradiol concentrations may be important in maintaining a female's reproductive state while males are chorusing. To our knowledge, this is the first study to demonstrate social regulation of estradiol concentration in female anurans.

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Section: Discussionmentioning

confidence: 99%

Social regulation of plasma estradiol concentration in a female anuran

Lynch

Wilczynski

2006

Hormones and Behavior

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“…To confirm mate receptivity, each female was tested once by using standard phonotaxis tests with whine and whine-chuck stimuli broadcast at 82 dB SPL (sound pressure level, relative to 20 P) from speakers at opposite sides of an acoustic chamber, then responsive females were placed inside sound-dampening boxes. After 2 h without stimulation, we exposed females to one of five acoustic treatments as described (30): silence, natural heterospecific P. enesefae call, natural P. pustulosus whine, natural P. pustulosus whine-chuck, or P. pustulosus chuck trimmed from the whine-chuck stimulus (Fig. 1).…”

Section: Methodsmentioning

confidence: 99%

“…We exposed females to one of five acoustic treatments: no stimulus, one of two irrelevant calls (conspecific chuck-only or heterospecific Physalaemus enesefae whine) or one of two behaviorally relevant calls (conspecific whine or whine-chuck). To determine the hypothalamic responses to these relevant and irrelevant calls, we examined mRNA levels of the activity marker egr-1 (also called krox-24, zif268, NGFI-A, TIS8, or ZENK) after acoustic stimulation (30). We measured egr-1 in seven hypothalamic nuclei (Fig.…”

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confidence: 99%

Social cues shift functional connectivity in the hypothalamus

Hoke

Ryan

Wilczynski

2005

Proc. Natl. Acad. Sci. U.S.A.

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We determined how social stimuli that vary in behavioral relevance differentially activate functional networks in the frog hypothalamus. As measured by egr-1 mRNA levels, activity in three hypothalamic nuclei varied with acoustic stimulus, and these responses were correlated with egr-1 responses in different auditory regions regardless of stimulus. The correlations among hypothalamic nuclei, however, varied as a function of the behavioral relevance of the stimuli. Thus relevant social cues shift the functional connectivity within the hypothalamus, consistent with principles that underlie the simultaneous processing of sensory information in cognitive tasks.amphibian ͉ immediate early gene ͉ mate choice ͉ neural network ͉ tú ngara frog T he complex anatomical connections characteristic of networks in the brain pose a challenge for understanding neural circuits and their dual capacities to motivate and respond to behavior. A traditional approach in studies of neural systems underlying social behavior has been to investigate properties of individual nuclei or centers. Alternatively, cognitive neuroscience studies have more recently focused on variation in the functional relationships among neocortical areas, that is, on network properties indicated by correlated patterns of activity among brain regions, or functional connectivity (1-3). Functional connectivity has been assessed by using metabolic measures such as positron emission tomography (1) or fluorodeoxyglucose incorporation (4) to infer neural activity patterns within brain networks.The limbic and hypothalamic areas are critical candidates for network analyses, because those nuclei are heavily and reciprocally interconnected anatomically and participate in complex ways in multiple aspects of behavior and physiology (5). The brain directs appropriate behavioral and physiological responses to diverse sensory inputs by partitioning interconnected brain regions into independent subnetworks that subserve different tasks (5). Newman (5) described the flexibility of functional connections involved in a variety of aggressive, sexual, and maternal behaviors in the context of a social behavior network of six limbic regions. A similar but not entirely congruent network of limbic regions has been described in geckos (6) in which developmental influences on functional connectivity have been linked to aggressive behaviors (7). Newman (5) predicted that sensory inputs modulate the transient subnetworks that mediate continuously varying behavioral responses to social cues. In this paper, we extend Newman's prediction to consider how socially relevant auditory inputs demarcate subnetworks in the hypothalamus, a brain division that has a critical role in mediating reproductive responses to social cues.Anurans are tractable models for such an investigation. Behavioral responses to conspecific vocal signals are well documented, and we have a rich understanding of how the auditory system differentially responds to behaviorally relevant acoustic stimuli (8,9). Neuroanatomical con...

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“…We processed brains of males for radioactive in situ hybridization to localize egr-1 mRNA, as previously described (Hoke et al, 2004;Hoke et al, 2007). We processed alternate sections of female brains, either for radioactive in situ hybridization against egr-1 or for TH immunocytochemistry, as follows.…”

Section: Tissue Processingmentioning

confidence: 99%

“…We used immediate-early gene egr-1 mRNA levels as a marker for neural (Hoke et al, 2004;Hoke, Ryan, & Wilczynski, 2005, and used immunohistochemistry for tyrosine hydroxylase (TH) protein as a marker for dopaminergic PT neurons. TH is an enzyme in the synthetic pathway shared by the catecholamines dopamine and norepinephrine.…”

Section: Introductionmentioning

confidence: 99%

Functional coupling between substantia nigra and basal ganglia homologues in amphibians.

Hoke¹,

Ryan²,

Wilczynski³

2007

Behavioral Neuroscience

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Neuroanatomical and pharmacological experiments support the existence of a homologue of the mammalian substantia nigra-basal ganglia circuit in the amphibian brain. Demarcation of borders between the striatum and pallidum in frogs, however, has been contentious, and direct evidence of functional coupling between the putative nigral and striatal homologues is lacking. To clarify basal ganglia function in anurans, the authors used expression of immediate-early gene egr-1 as a marker of neural activation in the basal ganglia of túngara frogs (Physalaemus pustulosus). Regional variation in egr-1 mRNA levels distinguished striatal and pallidal portions of the basal ganglia and supported the grouping of the striatopallidal transition zone with the dorsal pallidum. As further evidence for a functional coupling between the dopaminergic cells in the posterior tuberculum (the putative substantia nigra homologue) and the basal ganglia, a positive relationship was demonstrated between the size of the dopaminergic cell population and the neural activation levels within the dorsal pallidum. Keywordsanuran; basal ganglia; tyrosine hydroxylase; immediate-early gene expression; egr-1 Previous research has proposed that homologous basal ganglia circuits may exist in both amphibians and mammals (reviewed in Endepols, Schul, Gerhardt, & Walkowiak, 2004;Marín, Smeets, & González, 1998). The "direct" basal ganglia pathway in mammals involves a dopaminergic projection from the substantia nigra pars compacta (SNc) to the striatum. The output of the striatum inhibits activity in the pallidum and the substantia nigra pars reticulata (SNr), and output pathways from the pallidum and the SNr reach motor centers in the brainstem. Although details vary, this basic circuit appears to be an ancestral trait in tetrapods (Marín et al., 1998).In amphibians, the proposed homologous circuit to the mammalian nigrostriatal pathway includes the posterior tuberculum (PT), striatum, and dorsal pallidum. Catecholaminergic cells in the PT contain dopamine (González & Smeets, 1991) and project to the striatum (Marín, González, & Smeets, 1997b;Marín, Smeets, & González, 1997 analyses, these cells are proposed to be homologous to the dopaminergic SNc neurons in mammals (reviewed in Marín et al., 1998;Smeets & González, 2000). Chemoarchitecture and anatomical connections suggest that the amphibian basal ganglia consist of the homologues of the mammalian striatum (rostrally) and dorsal pallidum (caudally), with an intermediate portion that shares some characteristics with the striatum and other characteristics with the pallidum (Endepols, Schul, et al., 2004; Mülhenbrock-Lenter, Endepols, Roth, & Walkowiak, 2005; see also Marín, González, & Smeets, 1997c). Major outputs of the basal ganglia include direct and indirect paths to motor areas of the brainstem (Marín, González, & Smeets, 1997a;Wilczynski & Northcutt, 1983b).Functional similarities between mammalian and amphibian basal ganglia circuits exist as well.The dopaminergic projection to the striatu...

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Functional Mapping of the Auditory Midbrain during Mate Call Reception

Cited by 81 publications

References 53 publications

Social regulation of plasma estradiol concentration in a female anuran

Social regulation of plasma estradiol concentration in a female anuran

Social cues shift functional connectivity in the hypothalamus

Functional coupling between substantia nigra and basal ganglia homologues in amphibians.

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