Differential processing in modality‐specific Mauthner cell dendrites

Abstract

Animals process multimodal information for adaptive behavioural decisions. In fish, evasion of a diving bird that breaks the water surface depends on integrating visual and auditory stimuli with very different characteristics. How do neurons process such differential sensory inputs at the dendritic level? For that, we studied the Mauthner cells (M-cells) in the goldfish startle circuit, which receive visual and auditory inputs via two separate dendrites, both accessible for in vivo recordings. We investigated whether electrophysiological membrane properties and dendrite morphology, studied in vivo, play a role in selective sensory processing in the M-cell. The results obtained show that anatomical and electrophysiological differences between the dendrites combine to produce stronger attenuation of visually evoked postsynaptic potentials (PSPs) than to auditory evoked PSPs. Interestingly, our recordings showed also cross-modal dendritic interaction because auditory evoked PSPs invade the ventral dendrite (VD), as well as the opposite where visual PSPs invade the lateral dendrite (LD). However, these interactions were asymmetrical, with auditory PSPs being more prominent in the VD than visual PSPs in the LD. Modelling experiments imply that this asymmetry is caused by active conductances expressed in the proximal segments of the VD. The results obtained in the present study suggest modality-dependent membrane specialization in M-cell dendrites suited for processing stimuli of different time domains and, more broadly, provide a compelling example of information processing in single neurons.

Influence of Stimulus Intensity on Multimodal Integration in the Startle Escape System of Goldfish

“…M-cell in vivo recordings showed that back propagating visual and auditory postsynaptic synaptic potentials (PSPs) interact at the dendritic level (Medan et al, 2018). Also, M-cell dendrites possess membrane non-linearities that enhance the effectiveness of such PSPs (Faber and Korn, 1986; Medan and Preuss, 2014).…”

“…The latter notion however, does not exclude multimodal tectal neurons providing also critical input to the M-cell (Hiramoto and Cline, 2009; Truszkowski et al, 2017). Moreover, startle (i.e., M-cell) threshold is tightly controlled by at least two independent feedforward inhibition systems, which further influence sensory processing and multimodal integration (Preuss et al, 2006; Medan and Preuss, 2014; Medan et al, 2018). Together these findings suggest that a single neuron such as the M-cell can provide a neural correlate for the IEP phenomenon.…”

“…Integration of sensory information from different modalities is essential for decision-making of appropriately timed behavioral responses. In vertebrates, neurons processing multimodal inputs are found throughout the CNS, prominently the cortical sensory processing areas and superior colliculus in mammals (Meredith et al, 1987; Wallace et al, 1998; Ghazanfar and Schroeder, 2006; King and Walker, 2012), and the optic tectum and hindbrain in birds, amphibians, and fish (Winkowski and Knudsen, 2006; Hiramoto and Cline, 2009; Mu et al, 2012; Medan et al, 2018). Multimodal integration depends on overlapping timing and/or spatial location of unimodal stimuli and typically results in an enhancement of the neural and behavioral response.…”

Neuronal morphologies built for reliable physiology in a rhythmic motor circuit

“…To date, measuring voltage attenuation across the many neurite paths presented in complex neuronal structures using electrophysiological techniques has proven difficult. Thus, electrotonus has been experimentally assessed in only a handful of neuron types (for example: Spruston and Johnston, 1992; Spruston et al, 1994; Rapp et al, 1994; Carnevale et al, 1997; Stuart and Spruston, 1998; Chitwood et al, 1999; Jaffe and Carnevale, 1999; Otopalik et al, 2017b; Medan et al, 2018), and this greatly restricts our understanding of the breadth of biophysical organizations utilized in different neuron types and circuit contexts.…”

Mixing audio and video in dendrites

“…In this issue of The Journal of Physiology , Medan et al . () report on a study of the integration of combined sound and optic tectum stimulation on the dendrites of Mauthner cells. Using in vivo intracellular recordings, they elucidate much of the precise dendritic computation that occurs when these two sources of inputs are active.…”