Population coding strategies and involvement of the superior colliculus in the tactile orienting behavior of naked mole-rats.

Even simple behaviors of vertebrates are typically generated by the concerted action of large numbers of brain cells. However, the mechanisms by which groups of neurons work together as functional populations to guide behavior remain largely unknown. One of the major model systems for exploring these mechanisms has been mammalian visuomotor behavior. We describe here experiments that establish a new model system for analyzing the sensory control of behavior by neuronal populations using a mammalian somatosensory response: orientation to touch cues in a rodent. We found that the CNS mechanisms used to direct these orientation responses to touch can be delineated from behavioral experiments. In this study we demonstrate that the superior colliculus, a component of the vertebrate midbrain most often thought of as a visual structure, is an essential component of the naked mole-rat's unique tactile orienting behavior. Furthermore, the information processing that underlies this behavior displays striking parallels with that used for visual orientation at anatomical and computational levels.

The antennal system and cockroach evasive behavior. I. Roles for visual and mechanosensory cues in the response.

Cockroaches escape from predators by turning and then running. This behavior can be elicited when stimuli deflect one of the rostrally located and highly mobile antennae. We analyzed the behavior of cockroaches, under free-ranging conditions with videography or tethered in a motion tracking system, to determine (1) how antennal positional dynamics influence escape turning, and (2) if visual cues have any influence on antennal mediated escape. The spatial orientation of the long antennal flagellum at the time of tactile stimulation affected the direction of resultant escape turns. However, the sign of flagellar displacement caused by touch stimuli, whether it was deflected medially or laterally for example, did not affect the directionality of turns. Responsiveness to touch stimuli, and escape turn performance, were not altered by blocking vision. However, because cockroaches first orient an antenna toward stimuli entering the peripheral visual field, turn direction can be indirectly influenced by visual input. Finally, when vision was blocked, the run phase of escape responses displayed reduced average velocities and distances traveled. Our results suggest that tactile and visual influences are integrated with previously known wind-sensory mechanisms to achieve multisensory control of the full escape response.

The antennal system and cockroach evasive behavior. II. Stimulus identification and localization are separable antennal functions.

Cockroaches ( Periplaneta americana) orient their antennae toward moving objects based on visual cues. Presumably, this allows exploration of novel objects by the antennal flagellum. We used videographic and electrophysiological methods to determine if receptors on the flagellum are essential for triggering escape, or if they enable cockroaches to discriminate threatening from non-threatening objects that are encountered. When a flagellum was removed, and replaced with a plastic fiber, deflection of a "prosthetic flagellum" still activated the descending mechanosensory interneurons associated with escape and produced typical escape responses. However, escape was essentially eliminated by constraining the movement of the scape and pedicel at the antennal base. When cockroaches approached and briefly explored the surface of a spider or another cockroach with the flagellum, they produced escape significantly more often in response to subsequent controlled contact from a spider than from a cockroach. This discrimination did not depend on visual or wind-sensory input, but required flagellar palpation of the surface. The crucial sensory cues appear to involve texture rather than surface chemicals. These results indicate that cockroaches acquire basic information on stimulus identity during exploration of surfaces with flagellar receptors, but that basal receptors are triggers for escape behavior.

Identified nerve cells and insect behavior.

Studies of insect identified neurons over the past 25 years have provided some of the very best data on sensorimotor integration; tracing information flow from sensory to motor networks. General principles have emerged that have increased the sophistication with which we now understand both sensory processing and motor control. Two overarching themes have emerged from studies of identified sensory interneurons. First, within a species, there are profound differences in neuronal organization associated with both the sex and the social experience of the individual. Second, single neurons exhibit some surprisingly rich examples of computational sophistication in terms of (a) temporal dynamics (coding superimposed upon circadian and shorter-term rhythms), and also (b) what Kenneth Roeder called "neural parsimony": that optimal information can be encoded, and complex acts of sensorimotor coordination can be mediated, by small ensembles of cells. Insect motor systems have proven to be relatively complex, and so studies of their organization typically have not yielded completely defined circuits as are known from some other invertebrates. However, several important findings have emerged. Analysis of neuronal oscillators for rhythmic behavior have delineated a profound influence of sensory feedback on interneuronal circuits: they are not only modulated by feedback, but may be substantially reconfigured. Additionally, insect motor circuits provide potent examples of neuronal restructuring during an organism's lifetime, as well as insights on how circuits have been modified across evolutionary time. Several areas where future advances seem likely to occur include: molecular genetic analyses, neuroecological syntheses, and neuroinformatics--the use of digital resources to organize databases with information on identified nerve cells and behavior.

Cellular organization of an antennal mechanosensory pathway in the cockroach, Periplaneta americana.

Escape responses of cockroaches, Periplaneta americana, can be triggered by wind and mediated by a group of "giant interneurons" that ascend from cercal mechanoreceptors to motor centers. Recently it has been observed that escape also can be triggered by tactile stimulation of the antennae, and it is then independent of the giant interneurons. Here we identify a descending antennal mechanosensory pathway that may account for escape. Cobalt backfills demonstrated that a limited number of cells in the head ganglia have axons that project through all three thoracic ganglia. Comparison with known wind-sensory pathways indicated that wind is not a reliable stimulus for activating descending antennal pathways. However, direct touch stimulation of an antenna reliably evoked short-latency responses in cells with axons in the cervical connectives. Intracellular recording and dye injection revealed members of this pathway, referred to as descending mechanosensory interneurons (DMIs). The two axons of largest diameter in the cervical connectives were found to belong to DMIs, and these large-caliber interneurons were studied in detail. One had a soma in the supraesophageal ganglion, and the other in the subesophageal ganglion. Both had extensive neuritic arborizations at the same level as the soma and axonal arbors in all three thoracic ganglia. Each of these DMIs exhibited short-latency responses to small antennal movements, demonstrated a degree of directional sensitivity, and rapidly conducted impulses to thoracic levels. These cells have properties suggesting that they play a role in a short-latency behavior such as touch-evoked escape.

Correspondence of escape-turning behavior with activity of descending mechanosensory interneurons in the cockroach, Periplaneta americana.

Two bilaterally paired mechanosensory neurons that respond to antennal touch stimulation recently have been described in the cockroach Periplaneta americana. Here chronic recordings were used to describe the activity of these interneurons in relation to behavior. Parallel intra/extracellular recording experiments showed that both pairs of previously identified descending mechanosensory interneurons (DMIs) were activated after touch stimulation of the antennae and before initiation of escape. On a trial-by-trial basis, the bilateral pattern of their activity was correlated with sensory input and behavior: when one antenna was touched, the contralateral DMI axons displayed impulses earlier and in greater numbers than their ipsilateral homologs; turns were made toward the side with greater DMI activity, i.e., away from the touched antenna. One parameter of DMI activity (the bilateral difference in number of DMI impulses) was correlated with the angular amplitude of turning. In the absence of touch stimulation, unilateral electrical stimulation of a cervical connective via the chronic electrodes produced turning movements similar to natural escape turning and of appropriate directionality. These results support the hypothesis that neural activity in DMIs is involved in the control of antennal touch-evoked escape, and they provide a basis for a model of DMI specification of the direction of escape turning.

A motion tracking system for simultaneous recording of rapid locomotion and neural activity from an insect.

We have adapted techniques for studying the locomotion of tethered insects to analysis of rapid directional movements such as escape behavior. We describe here a computer-based motion tracking system that allows an animal to turn and run as rapidly as it does under free-ranging conditions, and that samples fast enough to accurately reconstruct the movements. Furthermore, we have designed chronic electrodes that allow for simultaneous extracellular recording of the activity of interneurons related to behavior. We used this system to record the escape response of tethered cockroaches, Periplaneta americana, and compared the data with those obtained from high-speed videographic analysis of the same animals under free-ranging conditions. In the motion tracking system, animals were normally responsive to sensory input, and expressed directional escape turning responses. This system allows details of an entire escape response (initial turn and subsequent running) to be quantified. These behavioral details can now be correlated with the discharge of key interneurons on a trial-by-trial basis.

The wind-elicited escape response of cockroaches (Periplaneta americana) is influenced by lesions rostral to the escape circuit.

When the escape response of the cockroach (Periplaneta americana) is triggered by wind, it is mediated by the cercal-to-giant interneuron pathway and leg motor circuitry, within the abdominal and thoracic portions of the ventral nerve cord. We have found that a lesion rostral to the thorax (transection of a cervical connective) produces specific changes in wind-evoked escape. Lesioned animals reliably displayed short-latency responses to wind. However, the orientation of the initial turning component of escape was altered and the duration of subsequent running was reduced. Preliminary physiological study suggests that changes in the orientation of escape reflect changes in the integration of wind-sensory signals by thoracic circuitry. These findings imply that rostral centers influence sensorimotor integration underlying wind-evoked escape.

An antennal-derived mechanosensory pathway in the cockroach: descending interneurons as a substrate for evasive behavior.

Large amplitude units responding to intense winds or touch of the antennae were recorded extracellularly from the cervical connectives of the cockroach, Periplaneta americana. Intracellular recording and staining revealed a number of interneurons with cell bodies in one of the head ganglia and large caliber axons descending to thoracic levels. These cells respond to touch of an antenna at very short latencies. The properties of these cells suggest that in the cockroach they may be a substrate for non-GI evasive behavior, especially for responses to predators which are detected by tactile cues.

Escape responses following elimination of the giant interneuron pathway in the cockroach, Periplaneta americana.

The entire set of giant interneurons (GIs) in the nerve cord of the cockroach, Periplaneta americana, was ablated using either electrolytic or surgical techniques. All animals with these lesions were capable of turning and running away from standard wind puffs. However, all animals responded much less frequently to standard wind stimuli following lesion, and the latency of their responses was significantly increased. These results are discussed in terms of a GI role in extremely short latency escape responses, and the idea that non-GI pathways, perhaps associated with head sensory structures, need to be considered in the normal control of escape in the cockroach.

Analyzing cockroach escape behavior with lesions of individual giant interneurons.

Individual giant interneurons (GIs) in the ventral nerve cord of the cockroach, Periplaneta americana, were lesioned by intracellular injection of proteolytic enzymes (pronase). This was accomplished with minimal dissection, so that the wind-evoked escape behavior of the animals could be studied following the lesion. Unilateral lesions of GI-2 had no obvious effect on escape behavior, but unilateral removal of GI-1, as well as combined unilateral lesions of GIs 1 and 2, influenced the direction of an animal's initial turning movement in response to a wind puff. These results support the hypothesis that GIs play a role in initiating and guiding the directional, wind-evoked escape response of the cockroach.