Joshua P. Martin

The neurobiology of insect olfaction: sensory processing in a comparative context.

The simplicity and accessibility of the olfactory systems of insects underlie a body of research essential to understanding not only olfactory function but also general principles of sensory processing. As insect olfactory neurobiology takes advantage of a variety of species separated by millions of years of evolution, the field naturally has yielded some conflicting results. Far from impeding progress, the varieties of insect olfactory systems reflect the various natural histories, adaptations to specific environments, and the roles olfaction plays in the life of the species studied. We review current findings in insect olfactory neurobiology, with special attention to differences among species. We begin by describing the olfactory environments and olfactory-based behaviors of insects, as these form the context in which neurobiological findings are interpreted. Next, we review recent work describing changes in olfactory systems as adaptations to new environments or behaviors promoting speciation. We proceed to discuss variations on the basic anatomy of the antennal (olfactory) lobe of the brain and higher-order olfactory centers. Finally, we describe features of olfactory information processing including gain control, transformation between input and output by operations such as broadening and sharpening of tuning curves, the role of spiking synchrony in the antennal lobe, and the encoding of temporal features of encounters with an odor plume. In each section, we draw connections between particular features of the olfactory neurobiology of a species and the animals life history. We propose that this perspective is beneficial for insect olfactory neurobiology in particular and sensory neurobiology in general.

Central-Complex Control of Movement in the Freely Walking Cockroach

To navigate in the world, an animals brain must produce commands to move, change direction, and negotiate obstacles. In the insect brain, the central complex integrates multiple forms of sensory information and guides locomotion during behaviors such as foraging, climbing over barriers, and navigating to memorized locations. These roles suggest that the central complex influences motor commands, directing the appropriate movement within the current context. Such commands are ultimately carried out by the limbs and must therefore interact with pattern generators and reflex circuits that coordinate them. Recent studies have described how neurons of the central complex encode sensory information: neurons subdivide the space around the animal, encoding the direction or orientation of stimuli used in navigation. Does a similar central-complex code directing movement exist, and if so, how does it effect changes in the control of limbs? Recording from central-complex neurons in freely walking cockroaches (Blaberus discoidalis), we identified classes of movement-predictive cells selective for slow or fast forward walking, left or right turns, or combinations of forward and turning speeds. Stimulation through recording wires produced consistent trajectories of forward walking or turning in these animals, and those that elicited turns also altered an inter-joint reflex to a pattern resembling spontaneous turning. When an animal transitioned to climbing over an obstacle, the encoding of movement in this new context changed for a subset of cells. These results indicate that encoding of movement in the central complex participates in motor control by a distributed, flexible code targeting limb reflex circuits.

Olfactory modulation by dopamine in the context of aversive learning

The need to detect and process sensory cues varies in different behavioral contexts. Plasticity in sensory coding can be achieved by the context-specific release of neuromodulators in restricted brain areas. The context of aversion triggers the release of dopamine in the insect brain, yet the effects of dopamine on sensory coding are unknown. In this study, we characterize the morphology of dopaminergic neurons that innervate each of the antennal lobes (ALs; the first synaptic neuropils of the olfactory system) of the moth Manduca sexta and demonstrate with electrophysiology that dopamine enhances odor-evoked responses of the majority of AL neurons while reducing the responses of a small minority. Because dopamine release in higher brain areas mediates aversive learning we developed a naturalistic, ecologically inspired aversive learning paradigm in which an innately appetitive host plant floral odor is paired with a mimic of the aversive nectar of herbivorized host plants. This pairing resulted in a decrease in feeding behavior that was blocked when dopamine receptor antagonists were injected directly into the ALs. These results suggest that a transient dopaminergic enhancement of sensory output from the AL contributes to the formation of aversive memories. We propose a model of olfactory modulation in which specific contexts trigger the release of different neuromodulators in the AL to increase olfactory output to downstream areas of processing.

Innate Recognition of Pheromone and Food Odors in Moths: A Common Mechanism in the Antennal Lobe?

The survival of an animal often depends on an innate response to a particular sensory stimulus. For an adult male moth, two categories of odors are innately attractive: pheromone released by conspecific females, and the floral scents of certain, often co-evolved, plants. These odors consist of multiple volatiles in characteristic mixtures. Here, we review evidence that both categories of odors are processed as sensory objects, and we suggest a mechanism in the primary olfactory center, the antennal lobe (AL), that encodes the configuration of these mixtures and may underlie recognition of innately attractive odors. In the pheromone system, mixtures of two or three volatiles elicit upwind flight. Peripheral changes are associated with behavioral changes in speciation, and suggest the existence of a pattern recognition mechanism for pheromone mixtures in the AL. Moths are similarly innately attracted to certain floral scents. Though floral scents consist of multiple volatiles that activate a broad array of receptor neurons, only a smaller subset, numerically comparable to pheromone mixtures, is necessary and sufficient to elicit behavior. Both pheromone and floral scent mixtures that produce attraction to the odor source elicit synchronous action potentials in particular populations of output (projection) neurons (PNs) in the AL. We propose a model in which the synchronous output of a population of PNs encodes the configuration of an innately attractive mixture, and thus comprises an innate mechanism for releasing odor-tracking behavior. The particular example of olfaction in moths may inform the general question of how sensory objects trigger innate responses.

Synchronous firing of antennal-lobe projection neurons encodes the behaviorally effective ratio of sex-pheromone components in male Manduca sexta

Olfactory stimuli that are essential to an animal’s survival and reproduction are often complex mixtures of volatile organic compounds in characteristic proportions. Here, we investigated how these proportions are encoded in the primary olfactory processing center, the antennal lobe, of male Manduca sexta moths. Two key components of the female’s sex pheromone, present in an approximately 2:1 ratio, are processed in each of two neighboring glomeruli in the macroglomerular complex (MGC) of males of this species. In wind-tunnel flight experiments, males exhibited behavioral selectivity for ratios approximating the ratio released by conspecific females. The ratio between components was poorly represented, however, in the firing-rate output of uniglomerular MGC projection neurons (PNs). PN firing rate was mostly insensitive to the ratio between components, and individual PNs did not exhibit a preference for a particular ratio. Recording simultaneously from pairs of PNs in the same glomerulus, we found that the natural ratio between components elicited the most synchronous spikes, and altering the proportion of either component decreased the proportion of synchronous spikes. The degree of synchronous firing between PNs in the same glomerulus thus selectively encodes the natural ratio that most effectively evokes the natural behavioral response to pheromone.

Extracellular wire tetrode recording in brain of freely walking insects

Increasing interest in the role of brain activity in insect motor control requires that we be able to monitor neural activity while insects perform natural behavior. We previously developed a technique for implanting tetrode wires into the central complex of cockroach brains that allowed us to record activity from multiple neurons simultaneously while a tethered cockroach turned or altered walking speed. While a major advance, tethered preparations provide access to limited behaviors and often lack feedback processes that occur in freely moving animals. We now present a modified version of that technique that allows us to record from the central complex of freely moving cockroaches as they walk in an arena and deal with barriers by turning, climbing or tunneling. Coupled with high speed video and cluster cutting, we can now relate brain activity to various parameters of the movement of freely behaving insects.

Introducing MantisBot: Hexapod robot controlled by a high-fidelity, real-time neural simulation

We present MantisBot, a 28 degree of freedom robot controlled by a high-fidelity neural simulation. It is modeled after the mantis, with many degrees of freedom, because we intend to study directed behaviors and leg multi-functionality, such as prey tracking and striking. As a first step, we present a distributed reflexive posture controller. MantisBot maintains posture through a series of reflexes observed in insects, specifically: strain measurements from a leg produce proportional torque commands (reflex A); large or rapidly decreasing leg strains produce a rapid, single “restep” (reflex B); a leg can only restep if its neighboring legs are all under strain (reflex C); and a leg will search for the ground if it does not reach it as expected (reflex D). All of these reflexes contribute to a hardware platforms posture, and are implemented in a highly distributed fashion. The two most distal joints in each leg each has its own central pattern generator (CPG, 12 total), upon which all of these behaviors depend. To achieve the desired dynamics, we implement a control network of conductance-based neurons with persistent sodium channels arranged in a network like the animal may possess in its thoracic ganglia. The result is a robot capable of actively maintaining posture without a centralized planner or body model. In addition, the network implementation is fast, calculating network dynamics 150 times faster than real time.

MantisBot: A Platform for Investigating Mantis Behavior via Real-Time Neural Control

We present Mantisbot, a 28 degree of freedom robot controlled in real-time by a neural simulation. MantisBot was designed as a 13.3:1 model of a male Tenodera sinensis with the animals predominant degrees of freedom. The purpose of this robot is to investigate two main topics: 1. the control of targeted motion, such as prey-directed pivots and striking, and 2. the role of descending commands in transitioning between behaviors, such as standing, prey stalking, and walking. In order to more directly use data from the animal, the robot mimics its kinematics and range of motion as closely as possible, uses strain gages on its legs to measure femoral strain like insects, and is controlled by a realistic neural simulation of networks in the thoracic ganglia. This paper summarizes the mechanical, electrical, and software design of the robot, and how its neural control system generates reflexes observed in insects. It also presents preliminary results; the robot is capable of supporting its weight on four or six legs, and using sensory information for adaptive and corrective reflexes.

Olfaction in Invertebrates: Manduca

Current knowledge of the olfactory system of Manduca sexta is discussed within the context of the natural history of this model organism. The anatomy of the olfactory system is described progressing from the antennas to the antennal lobes and then to higher centers of olfactory processing in the brain. The principles of olfactory information processing revealed from studies of this organism are discussed with respect to its ability to identify odors and evaluate their concentration and spatiotemporal dynamics. The cellular substrate underlying multiple functional roles of antennal lobe circuitry is also described.

Neuromechanical Mantis Model Replicates Animal Postures via Biological Neural Models

A neuromechanical model of a mantis was developed to explore the neural basis of some elements of hunting behavior, which is very flexible and context-dependent, for robotic control. In order to capture the complexity and flexibility of insect behavior, we have leveraged our previous work [1] and constructed a dynamical model of a mantis with a control system built from dynamical neuron models, which simulate the flow of ions through cell membranes. We believe that this level of detail will provide more insight into what makes the animal successful than a finite state machine (FSM) or a recurrent neural network (RNN). Each of the model’s walking legs has six degrees of freedom. Each joint is actuated by an antagonistic pair of muscles, controlled by a custom designed variable-stiffness joint controller based on insect neurobiology. The resulting low-level control system serves as the groundwork for a more complete behavioral model of the animal.