Temporal precision and reliability in the velocity regime of a hair-cell sensory system: the mechanosensory lateral line of goldfish, Carassius auratus

Goulet J, van Hemmen JL, Jung SN, Chagnaud BP, Scholze B, Engelmann J. Temporal precision and reliability in the velocity regime of a hair-cell sensory system: the mechanosensory lateral line of goldfish, Carassius auratus. Journal of neurophysiology. 2012;107(10):2581-2593.Fish and aquatic frogs detect minute water motion by means of a specialized mechanosensory system, the lateral line. Ubiquitous in fish, the lateral-line system is characterized by hair-cell based sensory structures across the fish's surface called neuromasts. These neuromasts occur free-standing on the skin as superficial neuromasts (SN) or are recessed into canals as canal neuromasts. SNs respond to rapid changes of water velocity in a small layer of fluid around the fish, including the so-called boundary layer. Although omnipresent, the boundary layer's impact on the SN response is still a matter of debate. For the first time using an information-theoretic approach to this sensory system, we have investigated the SN afferents encoding capabilities. Combining covariance analysis, phase analysis, and modeling of recorded neuronal responses of primary lateral line afferents, we show that encoding by the SNs is adequately described as a linear, velocity-responsive mechanism. Afferent responses display a bimodal distribution of opposite Wiener kernels that likely reflected the two hair-cell populations within a given neuromast. Using frozen noise stimuli, we further demonstrate that SN afferents respond in an extremely precise manner and with high reproducibility across a broad frequency band (10-150 Hz), revealing that an optimal decoder would need to rely extensively on a temporal code. This was further substantiated by means of signal reconstruction of spike trains that were time shifted with respect to their original. On average, a time shift of 3.5 ms was enough to diminish the encoding capabilities of primary afferents by 70%. Our results further demonstrate that the SNs' encoding capability is linearly related to the stimulus outside the boundary layer, and that the boundary layer can, therefore, be neglected while interpreting lateral line response of SN afferents to hydrodynamic stimuli

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