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Time disparity sensitive behavior and its neural substrates of a pulse-type gymnotiform electric fish, Brachyhypopomus gauderio

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Abstract

Roles of the time coding electrosensory system in the novelty responses of a pulse-type gymnotiform electric fish, Brachyhypopomus, were examined behaviorally, physiologically, and anatomically. Brachyhypopomus responded with the novelty responses to small changes (100 μs) in time difference between electrosensory stimulus pulses applied to different parts of the body, as long as these pulses were given within a time period of ~500 μs. Physiological recording revealed neurons in the hindbrain and midbrain that fire action potentials time-locked to stimulus pulses with short latency (500–900 μs). These time-locked neurons, along with other types of neurons, were labeled with intracellular and extracellular marker injection techniques. Light and electron microscopy of the labeled materials revealed neural connectivity within the time coding system. Two types of time-locked neurons, the pear-shaped cells and the large cells converge onto the small cells in a hypertrophied structure, the mesencephalic magnocellular nucleus. The small cells receive a calyx synapse from a large cell at their somata and an input from a pear-shaped cell at the tip of their dendrites via synaptic islands. The small cells project to the torus semicircularis. We hypothesized that the time-locked neural signals conveyed by the pear-shaped cells and the large cells are decoded by the small cells for detection of time shifts occurring across body areas.

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Abbreviations

ABC:

Avidin-biotin complex

DAB:

Diaminobenzidine

ELL:

Electrosensory lateral line lobe

EM:

Electron microscopy or electron micrograph

EOD:

Electric organ discharge

GA:

Glutaraldehyde

LM:

Light microscopy or light micrograph

MMN:

Mesencephalic magnocellular nucleus

PB:

Phosphate buffer

PBS:

Phosphate buffer saline

PFA:

Paraformaldehyde

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Acknowledgments

We thank two anonymous referees for critical reading of the manuscript. This work was supported by a grant from National Science Foundation IOS-0723356 to MK, and by the JSPS (Japan Society for the Promotion of Science) Grants-in-Aid for Scientific Research no. 22570073, and by a grant from the CPIS (Sokendai Center for the Promotion of Integrated Sciences) to AM. We also thank to Kentaro Arikawa for providing us with experimental space and equipment for anatomical studies. The histological materials other than those of Brachyhypopomus were prepared by Grace Kennedy and other members of Walter Heiligenberg’s laboratory in early 1990 s and donated to MK. All experiments were approved by the University of Virginia Animal Care Committee.

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Authors and Affiliations

  1. Department of Evolutionary Studies of Biosystems, Sokendai (The Graduate University for Advanced Studies), Hayama, 240-0193, Japan

    Atsuko Matsushita

  2. Department of Biology, University of Virginia, Charlottesville, VA, 22904, USA

    Grace Pyon & Masashi Kawasaki

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  1. Atsuko Matsushita
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  2. Grace Pyon
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  3. Masashi Kawasaki
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Correspondence to Atsuko Matsushita.

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Fig. 6

Time-locked neurons are non-adaptive to high repetition rate of stimulus pulses. a Intracellular recording from a time-locked neuron showing one-to-one spike firing to a pulse train of 450 Hz. b Field potential in the MMN to doublet pulses separated by 2 ms. Note only slight reduction in amplitudes between field potentials indicated by two arrows. Asterisks show stimulus pulse artifacts. c The time interval between the two pulses in b was varied from 2 to 40 ms, and the magnitude of the field potential to the second pulse was normalized to the field potential to the first pulse. Results in one fish recorded at the ganglion and the MMN with normal amplitude and 15 times higher amplitude of stimulus pulses than the natural EOD (eps 325 KB)

Fig. 7

The pear-shaped cells. a–c, g–i show extracellularly labeled cells. a1 A 50-μm thick transverse section of the right side of the ELL. Somata of the pear-shaped cells are arranged in the layer I (black arrow). Their axons form a thick bundle running toward the midline (white arrow). a2 A magnified view of the box in a1. b An exceptional pear-shaped cell whose soma possessed a dendrite (arrow). c Two somata of labeled pear-shaped cells (inset), one of which was enlarged (asterisk). The soma is contacted by a calyx (C) terminal. Arrowheads indicate the interface of the contact. d A labeled calyx ending of an afferent nerve fiber embracing a soma of a pear-shaped cell (P). e Conventional EM showing chemical synapses (arrows) between an afferent terminal (Af) and a pear-shaped cell soma (P). f A somatic myelination (arrowheads) of a pear-shaped cell. Note that continuous myelination with the axon hillock (asterisk). g An axon bundle in the lateral lemniscus. h A transverse section more anterior to g. Axons of the pear-shaped cells running through the torus semicircularis (T) and terminating in the MMN (arrow). L, lateral lemniscus. i Other material showing axon bundles (arrowheads) of pear-shaped cells and their glomerular terminals in the MMN (eps 16642 KB)

Fig. 8

Glomerular terminals of pear-shaped cells in the MMN. a–d Intracellularly neurobiotin-injected terminals of pear-shaped cells in the MMN from four different materials. a A glomerular terminal. b Axonal branching observed at a deep location in the MMN. c1 Composite micrograph of projection processes of a pear-shaped cell. This terminal attached at least three large cells (short arrows). One of them is shown in c2 embedded in resin for EM (c3). Long arrows indicate densely glomerular terminals. c2 Resin-embedded vibratome section of the large cell soma in c1. The large cell soma (arrow) is attached by a labeled club ending (arrowhead). c3 EM view of the large cell (c2) (asterisk). The vacuole in the club ending is probably an artifact from tracer injection or following processing, because we have never seen it in the conventional EM. c4 An expanded view of the box in c3, showing two gap junctions (arrows). d1 Glomerular terminals of another pear-shaped cell. The glomerulus (arrow) was observed with EM (d2). d2 EM of the endings in a glomerulus (arrowheads), surrounded by membranous structures, synaptic island. d3 Enlarged view of the box in d2. Arrows indicate postsynaptic densities whose electron densities are a little thinner than that of the labeled presynaptic profile. Asterisks, postsynaptic elements (dendrites). e1 Conventional EM of a synaptic island. Asterisks, fragments of postsynaptic dendrites. P, Presynaptic ending of a pear-shaped cell. e2 Magnified view of the box in e1, showing two asymmetric chemical synapses. Asterisks, postsynaptic dendrites (eps 12989 KB)

Fig. 9

The morphology of large cells. a A transverse section of the MMN (delineated with broken line) stained with neutral red showing distribution of somata of the large cells. Approximately 70 somata were counted in this section. Inset: Magnified view of two somata. b A myelinated soma and two club endings forming input synapses (asterisks). The boxed area in b is enlarged in c where gap junctions (arrowheads) and an adherence junction (arrow) are seen. C, Club ending, L, large cell. d1, d2 Camera Lucida drawings of individual large cells projected onto the transverse plane. The rostrocaudal dimension of the large cells in d1 and d2 are 650 and 750 μm, respectively. e A large cell soma (L) with two initial segments (asterisks) and two input terminals (arrows). The two input terminals attached on the unmyelinated part of the soma (L). Note the continuous myelination over the soma (arrowheads), initial segments, and axons. f Light micrograph of the large cell drawn in d2 showing the soma and proximal axon of an intracellularly labeled large cell in a single 50-μm thick section. s, soma. g, h Calyx endings of axon collaterals of the labeled large cell drawn in d2. i1–i3 Three sections sampled from serially cut ultrathin sections of a labeled calyx ending (arrowheads). Note that the ending embraces a soma of a postsynaptic neuron (asterisks) which has a dendrite (arrow) (eps 15105 KB)

Fig. 10

The small cells. a A small cell receiving a calyx-ending via gap junctions. Boxed area in a1 is enlarged in a2. Note the continuous gap junction. b Another small cell with a dendrite (arrowheads) and axon (asterisk). Portions of a calyx ending attached to the soma (arrows). c Retrogradely labeled small cells. Almost all labeled cells in the MMN were observed to have a dendrite and an axon. Short arrows indicate the tufted tip of dendrites. Arrowheads indicate bundles containing small cell axons. Long arrows: thick axons of pear-shaped cells. d A biocytin-labeled small cell with a dendrite (white arrowhead) and axon (black arrowhead). The end of the dendrite forms a tuft (thick arrow). Small arrow, axon of other small cell. Inset: The tufted dendritic tip of another small cell. e The tufted dendritic tip of a labeled small cell. e1 LM showing a tufted end (arrowhead) that was observed with EM (e2 and e3). Asterisk indicates the soma. e2 An ultrathin section showing a contact of labeled ends and an unlabeled axon terminal (P). Note laminated membranous structures (asterisks) around the labeled profile, indicating the ‘synaptic island’. Boxed area is enlarged in e3, showing numerous synaptic vesicles (arrowheads) (eps 7843 KB)

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Matsushita, A., Pyon, G. & Kawasaki, M. Time disparity sensitive behavior and its neural substrates of a pulse-type gymnotiform electric fish, Brachyhypopomus gauderio . J Comp Physiol A 199, 583–599 (2013). https://doi.org/10.1007/s00359-012-0784-4

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