Central processing of temperature information

Processing of temperature information is one of the least understood sensory functions of the insect brain. This depends partly on the low number of temperature receptor cells in comparison to photo-, mechano- or chemoreceptors, and partly on the location of temperature receptor cells in cuticular sensilla which are distributed on the body surface. However, a sensory system composed of a limited number of receptor cells which are responsive to physical changes of the surrounding environment that could be determined easily provides an advantage for studying mechanisms underlying neural information processing. We took advantage of these features and selected the insect temperature sense as our particular window into central nervous system information processing. Our data so far collected demonstrates that inputs from temperature and olfactory receptors converge onto individual neurons of the antennal lobe, the primary olfactory center. Bimodal convergence resulted in integrated responses to the simultaneous presentation of temperature and olfactory stimuli that are far different from those observed when each stimulus was presented alone. Beside integration of inputs from different sensory modalities, several neurons gave excitatory responses to both cooling and warming. This might seem quite baffling at first sight, because all temperature receptors display a discharge which is increased during cooling and decreased during warming. One has to conclude on a change in sign of the incoming temperature signal by channeling it through a neuron pool which provides disinhibition. In this way, a decrease in the cold cells` activity during warming may induce an increase in activity of antennal lobe neurons which is not provided by the cold receptor cells and so has a critical role in information processing in the nervous system. The field is now at a point where a leap of understanding will be achieved by 1. identification of neurons making up the temperature pathway, and 2. continued analysis of the information that is lost or retained in the passage from one synapse to the next along this pathway. The present project has this general aim in view.

All animals possess multiple sensory channels with which they can simultaneously sample a wide variety of physical changes in their environment. Because the highly adaptive and sen-sitive peripheral sensory organs that serve each channel are tuned to very different forms of energy, each animal can maximize its ability to detect changes in its world. However, by building parallel circuits in the brain in which modality-specific areas are complemented by regions in which inputs from the different senses converge on common neurons, evolution has provided an interesting duality. In some areas of the brain unique modality-specific impres-sions are produced, while in others, combinations of inputs are integrated to enhance the de-tection and reduce the ambiguity of the external events. In the present project, we sought to determine some of the consequences of multisensory convergence in the insect brain by using the cockroachs antennal lobe as a model to compare the effects of unimodal and multimodal stimulation. Individual neurons in the antennal lobe integrate information about warming or cooling with food-odor information. The integration generated by combined modality stimula-tion produced stronger responses than to each stimulus presented alone, or reduced the dis-charge evoked by a single modality stimulus. Thermoreceptive sensory cells provide information about both warming and cooling by responding with a high discharge rate to one direction of temperature change and with a low discharge rate to the other. The cockroach possess only one kind of thermoreceptive sensory cells, the cold cells which are excited during warming and inhibited during cooling. Warm coding inherent in the cold cells output is tapped separately to build warm-coded responses in specific neurons which are excited during warming. The fact that cold cells are designed to transmit warm information indicates that the decrease in discharge rate during warming is not only a byproduct of evolution s relentless search for high sensitivity to slowly fluctuating changes in temperature, but create the basis for a cold- opponent warm channel. The thermoreceptive sensory cells are used by ectothermic arthropods to regulate body temperature behaviorally. Thus they detect convective heat contained in ambient air. The thermal environment, however, is not only determined by air temperature but also by radiant heat. If both convective and radiant heat determine the thermoreceptors temperature, its re-sponse is ambiguous, not with regard to temperature but with regard to its source. The present experiments revealed that the design features of thermoreceptive sense organs limit their re- sponsiveness to radiant and specialize them for the detection of convective heat.