Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatus

Author Posting. © John Wiley & Sons, 2014. This is the author's version of the work. It is posted here by permission of John Wiley & Sons for personal use, not for redistribution. The definitive version was published in Journal of Comparative Neurology 522 (2014): 2887-2927, doi:10.1002/cne.23596.Although the neuroanatomical distribution of catecholaminergic (CA) neurons has been well documented across all vertebrate classes, few studies have examined CA connectivity to physiologically and anatomically identified neural circuitry that controls behavior. The goal of this study was to characterize CA distribution in the brain and inner ear of the plainfin midshipman fish (Porichthys notatus) with particular emphasis on their relationship with anatomically labeled circuitry that both produces and encodes social acoustic signals in this species. Neurobiotin labeling of the main auditory end organ, the saccule, combined with tyrosine hydroxylase immunofluorescence (TH-ir) revealed a strong CA innervation of both the peripheral and central auditory system. Diencephalic TH-ir neurons in the periventricular posterior tuberculum, known to be dopaminergic, send ascending projections to the ventral telencephalon and prominent descending projections to vocal–acoustic integration sites, notably the hindbrain octavolateralis efferent nucleus, as well as onto the base of hair cells in the saccule via nerve VIII. Neurobiotin backfills of the vocal nerve in combination with TH-ir revealed CA terminals on all components of the vocal pattern generator, which appears to largely originate from local TH-ir neurons but may include input from diencephalic projections as well. This study provides strong neuroanatomical evidence that catecholamines are important modulators of both auditory and vocal circuitry and acoustic-driven social behavior in midshipman fish. This demonstration of TH-ir terminals in the main end organ of hearing in a nonmammalian vertebrate suggests a conserved and important anatomical and functional role for dopamine in normal audition.National Institutes of Health; Grant number: SC2DA034996 (to P.M.F.); Grant sponsor: The Professional Staff Congress/ The City University of New York (PSC-CUNY); Grant number: 65650-00 43 (to P.M.F.); Grant sponsor: Leonard and Claire Tow Travel Award (to P.M.F.); Grant sponsor: Whitman Investigator Faculty Research Fellowships from the Marine Biological Laboratory, Woods, Hole, MA (where the study was partly conducted) (to P.M.F. and J.A.S.).2015-05-0

Catecholaminergic Innervation of Central and Peripheral Auditory Circuitry Varies with Reproductive State in Female Midshipman Fish, Porichthys notatus

In seasonal breeding vertebrates, hormone regulation of catecholamines, which include dopamine and noradrenaline, may function, in part, to modulate behavioral responses to conspecific vocalizations. However, natural seasonal changes in catecholamine innervation of auditory nuclei is largely unexplored, especially in the peripheral auditory system, where encoding of social acoustic stimuli is initiated. The plainfin midshipman fish, Porichthys notatus, has proven to be an excellent model to explore mechanisms underlying seasonal peripheral auditory plasticity related to reproductive social behavior. Recently, we demonstrated robust catecholaminergic (CA) innervation throughout the auditory system in midshipman. Most notably, dopaminergic neurons in the diencephalon have widespread projections to auditory circuitry including direct innervation of the saccule, the main endorgan of hearing, and the cholinergic octavolateralis efferent nucleus (OE) which also projects to the inner ear. Here, we tested the hypothesis that gravid, reproductive summer females show differential CA innervation of the auditory system compared to non-reproductive winter females. We utilized quantitative immunofluorescence to measure tyrosine hydroxylase immunoreactive (TH-ir) fiber density throughout central auditory nuclei and the sensory epithelium of the saccule. Reproductive females exhibited greater density of TH-ir innervation in two forebrain areas including the auditory thalamus and greater density of TH-ir on somata and dendrites of the OE. In contrast, non-reproductive females had greater numbers of TH-ir terminals in the saccule and greater TH-ir fiber density in a region of the auditory hindbrain as well as greater numbers of TH-ir neurons in the preoptic area. These data provide evidence that catecholamines may function, in part, to seasonally modulate the sensitivity of the inner ear and, in turn, the appropriate behavioral response to reproductive acoustic signals

Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior

Precise neuronal firing is especially important for behaviors highly dependent on the correct sequencing and timing of muscle activity patterns, such as acoustic signaling. Acoustic signaling is an important communication modality for vertebrates, including many teleost fishes. Toadfishes are well known to exhibit high temporal fidelity in synchronous motoneuron firing within a hindbrain network directly determining the temporal structure of natural calls. Here, we investigated how these motoneurons maintain synchronous activation. We show that pronounced temporal precision in population-level motoneuronal firing depends on gap junction-mediated, glycinergic inhibition that generates a period of reduced probability of motoneuron activation. Super-resolution microscopy confirms glycinergic release sites formed by a subset of adjacent premotoneurons contacting motoneuron somata and dendrites. In aggregate, the evidence supports the hypothesis that gap junction-mediated, glycinergic inhibition provides a timing mechanism for achieving synchrony and temporal precision in the millisecond range for rapid modulation of acoustic waveforms

Exposure to Advertisement Calls of Reproductive Competitors Activates Vocal-Acoustic and Catecholaminergic Neurons in the Plainfin Midshipman Fish, Porichthys notatus

While the neural circuitry and physiology of the auditory system is well studied among vertebrates, far less is known about how the auditory system interacts with other neural substrates to mediate behavioral responses to social acoustic signals. One species that has been the subject of intensive neuroethological investigation with regard to the production and perception of social acoustic signals is the plainfin midshipman fish, Porichthys notatus, in part because acoustic communication is essential to their reproductive behavior. Nesting male midshipman vocally court females by producing a long duration advertisement call. Females localize males by their advertisement call, spawn and deposit all their eggs in their mate’s nest. As multiple courting males establish nests in close proximity to one another, the perception of another male’s call may modulate individual calling behavior in competition for females. We tested the hypothesis that nesting males exposed to advertisement calls of other males would show elevated neural activity in auditory and vocal-acoustic brain centers as well as differential activation of catecholaminergic neurons compared to males exposed only to ambient noise. Experimental brains were then double labeled by immunofluorescence (-ir) for tyrosine hydroxylase (TH), an enzyme necessary for catecholamine synthesis, and cFos, an immediate-early gene product used as a marker for neural activation. Males exposed to other advertisement calls showed a significantly greater percentage of TH-ir cells colocalized with cFos-ir in the noradrenergic locus coeruleus and the dopaminergic periventricular posterior tuberculum, as well as increased numbers of cFos-ir neurons in several levels of the auditory and vocal-acoustic pathway. Increased activation of catecholaminergic neurons may serve to coordinate appropriate behavioral responses to male competitors. Additionally, these results implicate a role for specific catecholaminergic neuronal groups in auditory-driven social behavior in fishes, consistent with a conserved function in social acoustic behavior across vertebrates

Breakdown in the Smart City: Exploring Workarounds with Urban-sensing Practices and Technologies

Smart cities are now an established area of technological development and theoretical inquiry. Research on smart cities spans from investigations into its technological infrastructures and design scenarios, to critiques of its proposals for citizenship and sustainability. This article builds on this growing field, while at the same time accounting for expanded urban-sensing practices that take hold through citizen-sensing technologies. Detailing practice-based and participatory research that developed urban-sensing technologies for use in Southeast London, this article considers how the smart city as a large-scale and monolithic version of urban systems breaks down in practice to reveal much different concretizations of sensors, cities, and people. By working through the specific instances where sensor technologies required inventive workarounds to be setup and continue to operate, as well as moments of breakdown and maintenance where sensors required fixes or adjustments, this article argues that urban sensing can produce much different encounters with urban technologies through lived experiences. Rather than propose a “grassroots” approach to the smart city, however, this article instead suggests that the smart city as a figure for urban development be contested and even surpassed by attending to workarounds that account more fully for digital urban practices and technologies as they are formed and situated within urban projects and community initiatives

Seasonal differences in dopaminergic but not cholinergic innervation of the saccule, the main endorgan of hearing.

<p>(A, B) Transverse sections through the saccular epithelium. TH-ir and ChAT-ir puncta are largely concentrated at the base of hair cells and within the support cell layer. HC and SC labels point to DAPI-stained nuclei of individual hair cells and support cells, respectively. The rest of the hair cell is unlabeled and is a light purple background. Stereocillia (unlabeled) are located at the apical end of the hair cells. Quantification of numbers (C) and size (D) of putative TH-ir and ChAT-ir terminals (puncta) in the saccule (mean ± SE). Arrowhead in B indicates an example of a thick, varicose TH-ir fiber along the base of the SC layer that was excluded from the puncta analysis. Colors in the graphs match TH-ir and ChAT-ir in the micrographs. Mean number of puncta per image for animal in A = 41.4; B = 68.7. Mean area per punctum for animal A = 0.63 μm²; B = 0.78 μm². *<i>p</i> = 0.017, **<i>p</i> = 0.001. Scale bar = 25 μm.</p

Seasonal differences in TH-ir area but not cell number in the dopaminergic periventricular posterior tuberculum (TPp).

<p>(A, B) Large, pear-shaped TH-ir neurons and thick processes are seen just dorsal and lateral to the paraventricular organ (PVO) and medial to the medial forebrain bundle (MFB) along the midline in transverse section through the diencephalon. Data in C are expressed as number of TH-ir neurons per section (mean ± SE). (D) TH-ir area including cells and processes are quantified per unit area (143,139 μm²). Mean TH-ir area for animal in A = 6205.1μm²; B = 2658.4 μm². **<i>p</i> = 0.001. Scale bar = 100 μm.</p

Example micrographs showing no seasonal differences in TH-ir fiber density in transverse sections through (A, B) anterior tuberal hypothalamus (AT), (C, D) torus semicircularis (TS) and (D, E) ventral division of secondary octaval nucleus (SOv).

<p>Mean ± SE TH-ir density for summer vs. winter: AT (15.22% ± 0.74/ 11.68% ± 2.7); TS (16.30% ± 1.5/ 14.28% ± 1.0); SOv (4.12% ± 0.44/ 3.94% ± 0.25). Scale bar = 100 μm.</p

Seasonal differences in TH-ir fiber density in forebrain auditory nuclei.

<p>(A, B) central posterior nucleus of the thalamus (CP) and (D, E) lateral division of nucleus preglomerulosus (PGl). Left edge in A and B is midline of brain. Left edge in D and E is lateral edge of brain. Data in C and F are represented as percent area of the nucleus that contains TH-ir (mean ± SE). Mean TH-ir density for animal in A = 9.9%; B = 5.8%; D = 4.5%; E = 1.9%. *<i>p</i> = 0.03; *** <i>p</i> = 0.0003. Scale bar = 100 ¼m.</p