Robert OConnell, Ph.D.

Academic Role: Professor

Faculty Appointment(s) In:
   Physiology

Other Affiliation(s):
   Program in Neuroscience

Neurobiology of Olfaction

The ability of an organism's nervous system to detect and process information about the external world and then to generate appropriate behaviors is a prime factor in guaranteeing the organism's survival. We are interested in evaluating the physiological mechanisms that make it possible for the olfactory system to provide an organism with accurate information about certain volatile chemical signals (pheromones) in it's world.

The capabilities of the olfactory system are determined, as they are in other biological communication systems, by: 1) the nature and identity of the signals employed, 2) the receptor mechanisms that underlie signal transduction and encoding, 3) the processing and decoding of the resulting neural signals in the central nervous system and 4) the mechanisms that link these neural activities to the production of appropriate types of behavior. We assume that the physiological mechanisms that operate in primary olfactory receptor neurons so that they may detect and process pheromones, are good physiological models of the mechanisms that operate in all of the other chemically excitable neurons of the brain.

Vertebrate Pheromones

We examine olfactory communication in the mouse and hamster, because many aspects of their behavior are specifically determined by olfactory pheromones.

We have recently begun studies with a transgenic mouse (RAG-1) that cannot assemble the variable and constant portions of the genes responsible for generating immunoglobulins and T cell receptor molecules in developing lymphocytes. Since these molecules are necessary for the maturation of lymphocytes, RAG-1 deficient mice have no mature B and T lymphocytes and are severely immuno-compromised. In spite of this deficiency, RAG-1 mice mature and reproduce normally. Low levels of RAG-1 transcript have been detected in the mouse brain leading to the suggestion that RAG-1 deficient mice may have olfactory deficits because they are unable to assemble the variable and constant regions of olfactory receptor proteins. Preliminary behavioral tests of these animals have revealed a profound deficit in their olfactory preferences for certain natural sources of mouse pheromones. The genetic background of these animals has now been evaluated and found to be unremarkable, suggesting that the olfactory deficit is associated with the RAG phenotype. Additional anatomical, behavioral and physiological studies are planned to explore the olfactory systems of these, and other, interesting transgenic mice.

Invertebrate Pheromones

We study the physiological mechanisms of sex attraction and host-seeking behaviors in several important crop pests and vectors of human disease. In general, the capabilities of their olfactory receptor neurons appear less complex, and potentially easier to understand, than comparable neurons found in vertebrates. It may be that a knowledge of host-seeking and sexual orientation mechanisms will provide the information necessary for the design of efficient and ecologically safe methods of insect pest control.

We have recently begun an evaluation of the role of a particular class of olfactory receptor neuron in several species of mosquito including Aedes aegypti. Sensilla on the maxillary palps of females contain an olfactory receptor neuron which produces a phasic-tonic pattern of action potential response to low concentrations (150-300 ppm) of carbon dioxide, a stimulus known to be involved with host-seeking behavior. These receptor neurons (see Fig. 1) respond reliably to small increments in carbon dioxide concentration (50 ppm) likely to occur in nature. We assume that methods of insect control which exploit these and other sensory capabilities of the target animal are likely to be cost effective, amenable to relatively simple control measures, and should increase the public's overall degree of protection against mosquito borne diseases.

Figure 1. Average (plus and minus SEM) number of action potentials during 2 s stimulus pulses of the indicated concentrations of carbon dioxide from 13 receptor neurons in s. basiconica on the maxillary palps of 11 female Ae. aegypti. These responses were obtained in a synthetic air background containing 0 ppm CO2.

Selected Publications

O'Connell, R.J., Stevens, D.A. and Zogby, L.M. (1994). Individual differences in the perceived intensity and quality of specific odors following self- and cross-adaptation. Chemical Senses 19: 197-208.

Grant, A.J., Wigton, B., Aghajanian, J. and O'Connell, R.J. (1995). Electrophysiological responses to carbon dioxide from receptor neurons in mosquito maxillary palp sensilla, J. Comparative Physiology, A, 177: 389-396.

Stevens, D.A. and O'Connell, R.J. (1995). Enhanced sensitivity to androstenone following regular exposure to pemenone. Chemical Senses 20: 413-419.

Grant, A.J. and O'Connell, R.J. (1996). Electrophysiological responses from receptor neurons in mosquito maxillary palp sensilla, CIBA Symposium, 200: 233-253.

Grant, A.J., Borroni, P.F. and O'Connell, R.J. (1996). Different seasonal rearing conditions do not effect pheromone-sensitive receptor neurons of the adult cabbage looper moth. Trichoplusia ni. Physiological Entomology, 21: 59-63.

Stevens, D.A. and O'Connell, R.J. (1996) Semantic-free scaling of odor quality. Physiology and Behavior 60: 211-215.

Schoenfeld, T.A., Reasner, D.S. and O'Connell, R.J. (1996). Spatial patterns of neurogenesis in the olfactory epithelium of the adult mouse. Chemical Senses, Revised, 1997.

Kroner, C., Breer, H., Singer, A.G. and O'Connell, R.J. (1996) Pheromone-induced second messenger signaling in the hamster vomeronasal organ. Neuroreport, 7: 2989-2992.

Stevens, D.A. and O'Connell, R.J. (1996) Pemenone and androstenone do not cross-adapt reciprocally. Chemical Senses 21: 711-717.

Grant, A.J., Borroni, P.F. and O'Connell, R.J. , (1997). Pulsed pheromone stimuli affect the temporal response of antennal receptor neurons of the adult cabbage looper moth. Physiological Entomology, 22: 123- 130.

Clyne, P., Grant, A., O'Connell, R. and Carlson, JR (1997). Odorant response of individual sensilla on the Drosophila antenna. Invert. Neurosci. 3: 127-135.

Grant, A.J., Riendeau, C.J. and O'Connell, R.J. (1998). Spatial organization of olfactory receptor neurons on the antenna of the cabbage looper moth. J. Comparative Physiology, A 183: 433-442.

Academic Background

BS, LeMoyne College, 1963
Ph.D., SUNY Upstate, 1968

Pheromone Gated Channels

We continue to develop additional cellular and molecular approaches which will contribute to our long term goal of understanding the mechanisms of stimulus transduction in primary olfactory receptor neurons. We have developed techniques for isolating the apical membranes of olfactory and vomeronasal organ (VNO) receptor neurons from the hamster and the dendritic portion of olfactory receptor neurons from several insect species. In the hamster, we have shown that the cilia fraction from olfactory receptor neurons contains an odor-modulated adenylate cyclase enzyme system which may function as an amplifying stage in the signal transduction pathway. All of the isolated membranes fractions we have obtained contain a variety of integral single-channel proteins which seem to control current flow across the receptor neuron membrane. For example, membrane fragments from hamster VNO receptor neurons can be reconstituted into artificial lipid membranes where the electrical properties and chemical sensitivities of the channels in these membranes can be evaluated directly (see Fig. 2). In addition to the usual array of voltage sensitive channels to be expected in electrically excitable cells, this preliminary line of evidence indicates that VNO membranes also contain channels that gate current flow directly when they are exposed to the behaviorally relevant odors contained in extracts of HVD. It may be that directly-gated channels of this type play an important role in chemical transduction and the perception of olfactory pheromones.

Figure 2. Brief samples (120 ms/trace) of transmembrane current flows across a bilayer containing a channel reconstituted from microvilli removed from hamster vomeronasal receptor neurons. The first series of traces, on the top left, were obtained in an odor free solution. Those on the bottom right, were obtained after the addition of 300 micron-FE (Female Equivalents) of hamster vaginal discharge (HVD) extract to one side of the bilayer. Downward deflections indicate decreased current flow arising from the closing of an odor gated single channel. The current amplitude histograms illustrate the average size of the currents before and after the addition of HVD. Holding potential +45mV.

Office: Bryan 116
Phone: 508-856-5164
E-mail: Robert.OConnell@umassmed.edu

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