Sensory perception and aging in model systems: from the outside in

Abstract

Sensory systems provide organisms from bacteria to humans with the ability to interact with the world. Numerous senses have evolved that allow animals to detect and decode cues from sources in both their external and internal environments. Recent advances in understanding the central mechanisms by which the brains of simple organisms evaluate different cues and initiate behavioral decisions, coupled with observations that sensory manipulations are capable of altering organismal lifespan, have opened the door for powerful new research into aging. Although direct links between sensory perception and aging have been established only recently, here we discuss these initial discoveries and evaluate the potential for different forms of sensory processing to modulate lifespan across taxa. Harnessing the neurobiology of simple model systems to study the biological impact of sensory experiences will yield insights into the broad influence of sensory perception in mammals and may help uncover new mechanisms of healthy aging.

Figure 1. General schematic of sensory systems in Caenorhabditis elegans and Drosophila melanogaster

A) General organization of the C. elegans adult hermaphrodite nervous system, which consists of 302 neurons. The nerve ring is the main central nervous system neuropil in the worm, and it receives sensory input from the amphids at the anterior tip of the animal. Many sensory neurons terminate their primary axons in the nerve ring, and there is potential for sensory integration. Inset: Close up of select sensory neurons that may be relevant to aging. Cell bodies are shown in their approximate actual position and are organized by color according to function and/or effects on aging. B) General organization of the adult female Drosophila chemosensory system. As described in text, olfactory input is integrated in a geographically organized antennal lobe where distinct glomeruli receive inputs from olfactory neurons that express the same receptor (indicated by red, blue, or green neurons). Such organization is not apparent in the subesophageal ganglion (SOG), which receives taste inputs from a wide variety of taste receptor neurons. Motor neurons have been observed in the SOG but not the antennal lobe, which suggests the existence of local gustatory circuits that can drive behaviors independent of input from higher brain centers. Sensory signals are carried by second order projection neuron axons from both the SOG and antennal love to different regions of the brain, such as the mushroom bodies and lateral horn, where they are presumably integrated with metabolic and other information to influence changes in physiology and lifespan. Worm drawing were inspired and adapted from information in Worm Atlas (http://www.wormatlas.com). Fly line drawings are based directly on (Matsunami & Amrein 2004), while information and guidance for the Drosophila brain illustration was provided by FlyCircuit (http://www.flycircuit.tw).

Figure 2. Detecting, decoding and interpreting sensory input to modulate aging and physiology

Organisms are exposed to a wide-range of sensory stimuli from the environment. These inputs are detected by one or more peripheral sensory receptors that are tuned to specific ligands and that generate a characteristic set of neural responses in peripheral sensory neurons. Here, using the fly to illustrate phenomena that we believe are more general, we depict the processing of three hypothetical odorants (spider, fly, and banana) following their activation of three arbitrary sensory receptors (SR1, SR2, and SR3) to different degrees. The actual dimension of these spaces is much larger; flies, for example, express over sixty odorant receptors, while mice express over one-thousand. Neural signals from peripheral sensory neurons are processed in various types of integrative neuropil (e.g., the antennal lobe in flies, ring gland in worms, and olfactory bulb in mammals) to improve signal to noise ratio, maximize sensitivity, and enhance signal discrimination. Second-order neurons then pass the refined signals to higher regions of the brain (e.g., the mushroom bodies in flies and hypothalamus in mammals) where they are interpreted and perceived as ecologically relevant cues. From here, the cues may be integrated further with previous experience or with information about the nutritional and metabolic status of the organism, perhaps through internal sensory receptors. Very similar to behavior, the result may be to generate rapid and long-lasting effects on various aspects of organism physiology, including those that promote survival, reproductive output, and/or fat storage. We postulate that the mechanisms that are recruited to respond to perceived cues are evolutionary conserved “public” mechanisms, while those that are highly tuned to process specific signals are “private” and unique to each organism. Three-dimensional odor space diagrams are based on and expanded from ideas presented in Masse, Turner, and Jefferis (Masse et al 2009).