Elsevier

Brain Research

Volume 842, Issue 2, 25 September 1999, Pages 408-418
Brain Research

Research report
Histamine-immunoreactive neurons in the brain of the cockroach Leucophaea maderae

https://doi.org/10.1016/S0006-8993(99)01864-8Get rights and content

Abstract

Histamine is the neurotransmitter of insect photoreceptor cells but has also been found in a small number of interneurons in the insect brain. In order to investigate whether the accessory medulla (AMe), the putative circadian pacemaker of the cockroach Leucophaea maderae receives direct visual input from histaminergic photoreceptors, we analyzed the distribution of histamine-like immunoreactivity in the optic lobe and midbrain of the cockroach. Intense immunostaining was detected in photoreceptor cells of the compound eye, which terminated in the first optic neuropil, the lamina, and in a distal layer of the medulla, the second optic neuropil. Histamine immunostaining in parts of the AMe, however, originated from a centrifugal neuron of the midbrain. Within the midbrain 21–23 bilaterally symmetric pairs of cell bodies were stained. Most areas of the brain were innervated by one or more of these neurons, but the protocerebral bridge and the mushroom bodies were devoid of histamine immunoreactivity. The branching patterns of most histamine-immunoreactive neurons could be reconstructed individually. While the majority of identified neurons arborized in both brain hemispheres, five cells were local neurons of the antennal lobe. A comparison with other insect species shows striking similarities in the position of certain histamine-immunoreactive neurons, but considerable variations in the presence and branching patterns of others. The data suggest a role for histamine in a non-photic input to the circadian system of the cockroach.

Introduction

Histamine has been shown to be a neurotransmitter and/or neuromodulator in both vertebrates and invertebrates. In all vertebrates studied so far, histaminergic neurons reside exclusively in the hypothalamus and innervate most parts of the brain 17, 27. In invertebrates, histamine-immunoreactive neurons have been demonstrated in a flatworm [7], in a mollusc and in various arthropods. A histaminergic neuron in the opisthobranch mollusc Aplysia californica is involved in various aspects of feeding behavior [5]. In arthropods, physiological 4, 18, biochemical [32]and immunocytochemical 22, 28evidence strongly suggests that histamine is the transmitter of all known imaginal photoreceptor cells (reviews: Refs. 23, 39). Histamine released from photoreceptor neurons acts through chloride-mediated hyperpolarization of second order visual neurons in crustaceans as well as in insects [10]. In Drosophila melanogaster histamine was found to be the transmitter of certain mechanoreceptors as well 3, 22. Immunocytochemical studies in various insect species have further demonstrated the presence of histamine in a small number of neurons in the central nervous system 2, 15, 27, 29.

In the cockroach Leucophaea maderae, photoreceptors in the compound eyes are the only ones so far shown to be important for entrainment of the circadian rhythm of locomotor activity [26]. The circadian pacemaker of this insect is most likely located in the accessory medulla (AMe), a small neuropil at the anterior edge of the medulla in the optic lobe 11, 12, 34, 36. Intracellular recordings showed that neurons of the AMe of L. maderae react with a sustained response in spiking activity when the compound eyes are illuminated [19]. To investigate the possibility of direct innervation of the AMe by photoreceptor axons, as has been suggested in flies [25], we studied histamine immunostaining in the optic lobe and midbrain of the cockroach. We show that immunolabeling in the AMe of the cockroach originates from a centrifugal neuron of the protocerebrum, and present a detailed morphological study of histamine immunostaining in the midbrain, which allowed identification of this neuron.

Section snippets

Animals

Cockroaches of the species L. maderae FABRICIUS, 1792 (Blattodea, Blaberidae) were reared in a crowded laboratory culture in a 12 h light–dark cycle at 26°C. Adult males were taken at night and dissected under dim red light to prevent depletion of the neurotransmitter in photoreceptor cells.

Fixation and immunocytochemistry

Immunocytochemistry was performed on free-floating Vibratome sections by means of the indirect peroxidase–antiperoxidase (PAP) technique [37]. Brains and retinae were fixed with freshly prepared, ice cold 4%

Optic lobe

Histamine immunoreactivity in the optic lobe of L. maderae was concentrated in retinal photoreceptor cells. Immunostaining in the optic nerves and in the first optic neuropil, the lamina, where the majority of photoreceptors terminate, was particularly strong (Fig. 1a,c). A portion of immunostained photoreceptor fibers travelled across the outer chiasma and terminated within a distal layer of the medulla, where individual columns could be recognized by the pattern of histamine-immunoreactive

Discussion

In the brain of the cockroach L. maderae, we have demonstrated histamine immunostaining in photoreceptor cells of the compound eyes and, in addition, in a small number of widely dispersed interneurons. Most immunostained photoreceptors terminated in the lamina while a smaller number crossed the outer chiasma and innervated a distal layer of the medulla. This principal pattern of histamine-immunoreactive photoreceptor innervation applies to all hithereto investigated insect species: In the

Acknowledgements

Supported by DFG grant Ho 950/9.

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