Tyrosine hydroxylase immunolabeling reveals the distribution of catecholaminergic neurons in the central nervous systems of the spiders Hogna lenta (Araneae: Lycosidae) and Phidippus regius (Araneae: Salticidae)

Abstract

With over 48,000 species currently described, spiders (Arthropoda: Chelicerata: Araneae) comprise one of the most diverse groups of animals on our planet, and exhibit an equally wide array of fascinating behaviors. Studies of central nervous systems (CNSs) in spiders, however, are relatively sparse, and no reports have yet characterized catecholaminergic (dopamine [DA]‐ or norepinephrine‐synthesizing) neurons in any spider species. Because these neuromodulators are especially important for sensory and motor processing across animal taxa, we embarked on a study to identify catecholaminergic neurons in the CNS of the wolf spider Hogna lenta (Lycosidae) and the jumping spider Phidippus regius (Salticidae). These neurons were most effectively labeled with an antiserum raised against tyrosine hydroxylase (TH), the rate‐limiting enzyme in catecholamine synthesis. We found extensive catecholamine‐rich neuronal fibers in the first‐ and second‐order optic neuropils of the supraesophageal mass (brain), as well as in the arcuate body, a region of the brain thought to receive visual input and which may be involved in higher order sensorimotor integration. This structure likely shares evolutionary origins with the DA‐enriched central complex of the Mandibulata. In the subesophageal mass, we detected an extensive filigree of TH‐immunoreactive (TH‐ir) arborizations in the appendage neuromeres, as well as three prominent plurisegmental fiber tracts. A vast abundance of TH‐ir somata were located in the opisthosomal neuromeres, the largest of which appeared to project to the brain and decorate the appendage neuromeres. Our study underscores the important roles that the catecholamines likely play in modulating spider vision, higher order sensorimotor processing, and motor patterning.

The visual pathway in sea spiders (Pycnogonida) displays a simple serial layout with similarities to the median eye pathway in horseshoe crabs

“…This distinct set of catecholaminergic neurons underpins the relay of visual information from the VN to the AB already deduced by the presence of the connecting tract. Interestingly, in euchelicerates, a recent study of TH immunoreactivity in the brain of spiders has revealed a similarly extensive labeling for catecholamines in the VNs and several AB layers [ 70 ]. Further, histofluorescent visualization of catecholamines in the brain of xiphosurans has also indicated their presence in neurites of the AB and some VNs [ 88 ].…”

“…Tyrosine hydroxylase (TH) is the rate-limiting enzyme in the synthesis of catecholamines (dopamine, adrenaline, noradrenaline) [ 69 ], of which dopamine represents an important neurotransmitter in the arthropod nervous system. A monoclonal mouse antibody raised against purified TH from rat PC12 cells was used, having been prior to this study successfully applied in spiders [ 70 ].…”

“…Histamine is an inhibitory neurotransmitter utilized by photoreceptive cells across all major arthropod groups [ 61 – 68 ] and thus was expected to highlight the brain centers targeted by histamine-immunoreactive (histamine-ir) R-cell axon terminals. Beyond that, the distribution of tyrosine hydroxylase (TH), the rate-limiting enzyme in the biosynthesis of catecholamines (dopamine, adrenaline, noradrenaline) [ 69 ], was a priori considered a promising candidate for further characterization of the VNs and AB and their putative interconnections, as a recent study showed extensive TH-ir synaptic varicosities in these brain centers in spiders [ 70 ].…”

Single-cell transcriptomics reveals the brain evolution of web-building spiders

“…The unique structural characteristics related to web building, such as silk and mechanosensory sensilla, have garnered increased interest and detailed descriptions. However, only a small number of molecules (for example, neuropeptide) or neurons had been thoroughly described in spiders 49 . We found that most PSGs were highly expressed on the brain, indicating the key role of CNS in the evolution of spiders beyond the structure innovations.…”