Dept of Bioengineering, Imperial college London, London, U.K.
How is visual information processing related to the mode of locomotion? We may expect the state of locomotion, e.g. walking or flying, to impose different requirements on information processing regarding bandwidth, control system time constants and energy expenditure. We have explored the effects of Octopamine (OA) receptor activity, a putative component of the flight state, on information processing in the blowfly, C. vicina. OA is an invertebrate neurotransmitter, neuromodulator and neurohormone associated with ”fight or flight” responses in many species. OA haemolymph levels are elevated during flight in the cricket and locust, and the highest density of OA receptors is found in the optic lobes in the locust. We recorded extracellularly from spiking V1 and V2 cells, which belong to a population of motion-sensitive cells in the fly lobula plate. Both are most sensitive to vertical motion presented in the ipsilateral visual field and receive weaker input from the contralateral eye. We used periodic gratings to determine the directional tuning curves at specific locations in the cells’ receptive fields. The OA agonist chlordimeform (CDM) was applied, at a concentration of 2.6μM, high enough to significantly elevate the spontaneous spike rates of the cells. CDM increased the V1 cell spontaneous spike rate by a factor of 2.9, from 10.4 ±4.3 Hz to 27.0 ±6.4 Hz, and the V2 cell activity by a factor of 2.3, from 7.3 ±3.4 Hz to 16.4 ±5.6 Hz. CDM also elevated the information rate at which the direction of motion is encoded in both cells. We present increases over time windows sufficiently long to ensure significant non-zero increases. The V1 cell’s information rate was boosted by 55% over a 50ms window. The V2 information rate was increased by 24% over a 100ms window. Gains in the modulation depth of the directional tuning curve were offset by simultaneous increase of the response variabilites. The elevated spontaneous activity, however, allows both neurons to express more information about motion in the anti-preferred direction. CDM also decreased the mean response delay of the V2 cell by 6.0% from 23.4ms to 22.0ms, and that of the V1 cell by 4.4% from 21.4ms to 20.45ms. Our findings suggest that OA adapts the system to the higher dynamic range of stimuli during flight as opposed to walking by i) shortening the neural response delay, ii) elevating the spontaneous activity for a more efficient use of the negative response range and iii) increasing the modulation depth of the directional tuning curve. The higher efficiency in neural processing is reflected by an increase of the information rate for coding directional motion and comes at the expense of an increased metabolic cost.