Neural Representation of Object Approach in a Decision-Making Motor Circuit

Abstract

Although behavior is ultimately guided by decision-making neurons and their associated networks, the mechanisms underlying neural decision-making in a behaviorally relevant context remain mostly elusive. To address this question, we analyzed goldfish escapes in response to distinct visual looming stimuli with high-speed video and compared them with electrophysiological responses of the Mauthner cell (M-cell), the threshold detector that initiates such behaviors. These looming stimuli evoke powerful and fast body-bend (C-start) escapes with response probabilities between 0.7 and 0.91 and mean latencies ranging from 142 to 716 ms. Chronic recordings showed that these C-starts are correlated with M-cell activity. Analysis of response latency as a function of the different optical parameters characterizing the stimuli suggests response threshold is closely correlated to a dynamically scaled function of angular retinal image size, (t), specifically (t) ϭ (t Ϫ ␦ ϫ e Ϫ ␤ (t Ϫ ␦) , where the exponential term progressively reduces the weight of (t). Intracellular recordings show that looming stimuli typically evoked bursts of graded EPSPs with peak amplitudes up to 9 mV in the M-cell. The proposed scaling function (t) predicts the slope of the depolarizing envelope of these EPSPs and the timing of the largest peak. An analysis of the firing rate of presynaptic inhibitory interneurons suggests the timing of the EPSP peak is shaped by an interaction of excitatory and inhibitory inputs to the M-cell and corresponds to the temporal window in which the probabilistic decision of whether or not to escape is reached.

Relationship between the Phases of Sensory and Motor Activity during a Looming-Evoked Multistage Escape Behavior

“…It makes sense that locusts would ignore very slow approaches (high l/͉v͉) and might fail to generate an appropriate escape motor program in response to very fast approaching stimuli (low l/͉v͉). Decreased escape probabilities for small and fast stimuli have been reported in goldfish as well (Preuss et al, 2006). Thus, we believe that l/͉v͉ ϭ 40 -120 ms covers the range leading to the most relevant and robust escape jumps in the present context.…”

“…However, it does not rule out the involvement of other neurons in the generation of this motor program. Preuss et al (2006) have described recently looming-evoked escape responses in goldfish triggered by visual inputs to the Mauthner cell. Approaching objects elicit a compound EPSP (cEPSP) that has a similar, although not identical, time course to the DCMD firing rate: the cEPSP amplitude increases, peaks, and then decays toward the end of approach.…”

“…Some animals have evolved fast motor circuits devoted to the generation of such behaviors, such as the giant fiber system in flies, the Mauthner cell in fish, or the lateral giant neurons of crayfish (Wyman et al, 1984;Edwards et al, 1999;Korn and Faber, 2005). Although much is known in these and in other systems about how escape behaviors are generated in response to abrupt stimuli such as mechanical disturbances, air puffs, or light flashes (Levi and Camhi, 2000;Fayyazuddin et al, 2006;Bhatt et al, 2007), we still know very little about how escape behaviors are generated in response to objects approaching on a collision course, as may be expected from potential predators (Yamamoto et al, 2003;Preuss et al, 2006;Santer et al, 2006;Oliva et al, 2007;Hammond and O'Shea, 2007).…”

Massive increase in visual range preceded the origin of terrestrial vertebrates

“…Although this neural circuit enables ultrafast reactions to stimuli (≈4 ms), the limited number of neurons and synapses involved constrains the flexibility of the response (60). Mauthner command cells, activated by close-range acoustic, lateral line, tactile, and looming visual stimuli (59) in proportion to the speed of looming (61), are only present in vertebrates up through amphibians, including frogs (62,63).…”

Logarithmic Compression of Sensory Signals within the Dendritic Tree of a Collision-Sensitive Neuron

“…The peak firing rate always occurs a fixed delay after the time at which the looming stimulus reaches an angular threshold on the retina, independent of the stimulus' specific characteristics, such as the simulated object's size, speed, texture, or approach direction (Gabbiani et al, 1999;. Neurons with nearly identical response profiles have been identified in a variety of vertebrate and invertebrate species (Sun and Frost, 1998;Wu et al, 2005;Preuss et al, 2006;Fotowat et al, 2009;Nakagawa and Hongjian, 2010;Liu et al, 2011).…”