Gwen A. Jacobs

A reflex behavior mediated by monosynaptic connections between hair afferents and motoneurons in the larval tobacco hornworm, Manduca sexta.

Summary1.In the tobacco hornworm caterpillar, tactile stimulation of sensory hairs located on the tip of a proleg (the planta) evokes ipsilateral or bilateral retraction of the prolegs in that segment (Figs. 1,2). We have used electrophysiological and anatomical methods to investigate the excitatory neural pathways linking the planta hair afferents and the proleg retractor motoneurons (MNs). An important technical innovation was the development of an isolated proleg and desheathed ganglion preparation that permits rapid and reversible ionic manipulations and drug applications (Fig. 3).2.Action potentials (spikes) in individual planta hair afferents produce time-locked excitatory postsynaptic potentials (EPSPs) in ipsilateral proleg MNs (Fig. 3) which appear to be chemically-mediated and monosynaptic: the EPSPs have a short and constant latency, they follow afferent spikes without failure, they are reversibly abolished in elevated Mg++ saline (Fig. 7), and they persist in saline with elevated Mg++ and Ca++ levels (Fig. 8). Planta hair afferents also excite ipsilateral MNs by polysynaptic pathways, and their excitation of contralateral proleg MNs is exclusively polysynaptic.3.Cobalt-staining of the proleg MNs and planta hair afferents (Fig. 6) shows that the afferents terminate in ventral neuropil, and the proleg MNs have an unusual ventral projection into this region. The ventral projection is on the ipsilateral side, which is consistent with the electrophysiological finding that time-locked EPSPs are found only from ipsilateral hairs.4.Two factors that contribute to the strong monosynaptic excitation of proleg MNs by ipsilateral planta hairs are the convergence of many hair afferents onto each MN (Fig. 5), and the facilitation shown at each afferent-MN synapse (Fig. 9). At least 6 afferents converge on each MN, and at short interspike intervals the afferent-evoked EPSPs are enhanced by as much as 400% by homosynaptic facilitation.5.The EPSP is abolished reversibly by the cholinergic antagonists curare and atropine (Fig. 10), suggesting that the neurotransmitter at the synapse is acetylcholine (ACh). This is of particular interest because the ACh receptors of tobacco-feedingManduca larvae are reported to be less nicotinesensitive than those of other insects.

Towards effective and rewarding data sharing.

Recently issued NIH policy statement and implementation guidelines (National Institutes of Health, 2003) promote the sharing of research data. While urging that “all data should be considered for data sharing” and “data should be made as widely and freely available as possible” the current policy requires only high-direct-cost (>US

Computational mechanisms of mechanosensory processing in the cricket

500,000/yr) grantees to share research data, starting 1 October 2003. Data sharing is central to science, and we agree that data should be made available.

Direction sensitivity of the filiform hair population of the cricket cereal system

SUMMARY Crickets and many other orthopteran insects face the challenge of gathering sensory information from the environment from a set of multi-modal sensory organs and transforming these stimuli into patterns of neural activity that can encode behaviorally relevant stimuli. The cercal mechanosensory system transduces low frequency air movements near the animals body and is involved in many behaviors including escape from predators, orientation with respect to gravity, flight steering, aggression and mating behaviors. Three populations of neurons are sensitive to both the direction and dynamics of air currents: an array of mechanoreceptor-coupled sensory neurons, identified local interneurons and identified projection interneurons. The sensory neurons form a functional map of air current direction within the central nervous system that represents the direction of air currents as three-dimensional spatio-temporal activity patterns. These dynamic activity patterns provide excitatory input to interneurons whose sensitivity and spiking output depend on the location of the neuronal arbors within the sensory map and the biophysical and electronic properties of the cell structure. Sets of bilaterally symmetric interneurons can encode the direction of an air current stimulus by their ensemble activity patterns, functioning much like a Cartesian coordinate system. These interneurons are capable of responding to specific dynamic stimuli with precise temporal patterns of action potentials that may encode these stimuli using temporal encoding schemes. Thus, a relatively simple mechanosensory system employs a variety of complex computational mechanisms to provide the animal with relevant information about its environment.

Dendritic Design Implements Algorithm for Synaptic Extraction of Sensory Information

Each cercus on the adult cricket Acheta domesticus bears 1000–2000 filiform hair mechanoreceptors. In order to determine the extent of “identifiability” of individual hair receptors, the structural characteristics of ten putative identified hairs were measured in 21–25 different animals. For these ten hairs, the sets of preferred directions and circumferential locations had standard deviations of 6.8° and 5.9°, respectively. There was no significant inter-animal covariance between a hairs preferred direction and its circumferential location. The preferred directions of 246 different identified hairs were then measured from 16 animals in order to characterize the distribution of preferred directions of hairs on a single typical cercus. These data were transformed from the frame of reference of the cercus into that of the cricket, generating an estimate of the representation of air-current stimulus direction provided by the entire ensemble of filiform hairs on both cerci. The distribution of hair directional sensitivities was continuous but extremely non-uniform, and more complex than previous studies had suggested.

Anatomy and physiology of identified wind-sensitive local interneurons in the cricket cercal sensory system

While sensory information is encoded by firing patterns of individual sensory neurons, it is also represented by spatiotemporal patterns of activity in populations of the neurons. Postsynaptic interneurons decode the population response and extract specific sensory information. This extraction of information represented by presynaptic activities is a process critical to defining the input–output function of postsynaptic neuron. To understand the “algorithm” for the extraction, we examined directional sensitivities of presynaptic and postsynaptic Ca2+ responses in dendrites of two types of wind-sensitive interneurons (INs) with different dendritic geometries in the cricket cercal sensory system. In IN 10-3, whose dendrites arborize with various electrotonic distances to the spike-initiating zone (SIZ), the directional sensitivity of dendritic Ca2+ responses corresponded to those indicated by Ca2+ signals in presynaptic afferents arborizing on that dendrite. The directional tuning properties of individual dendrites varied from each other, and the directional sensitivity of the nearest dendrite to the SIZ dominates the tuning properties of the spiking response. In IN 10-2 with dendrites isometric to the SIZ, directional tuning properties of different dendrites were similar to each other, and each response property could be explained by the directional profile of the spatial overlap between that dendrite and Ca2+-elevated presynaptic terminals. For IN 10-2, the directional sensitivities extracted by the different dendritic-branches would contribute equally to the overall tuning. It is possible that the differences in the distribution of synaptic weights because of the dendritic geometry are related to the algorithm for extraction of sensory information in the postsynaptic interneurons.

Structural and biophysical mechanisms underlying dynamic sensitivity of primary sensory interneurons in the cricket cercal sensory system

Summary1.A group of wind sensitive local interneurons (9DL Interneurons) in the terminal abdominal ganglion of the cricket Acheta domesticus were identified and studied using intracellular staining and recording techniques.2.The 9DL interneurons had apparent resting potentials ranging from -38 mV to -45 mV. At this membrane potential, these cells produced graded responses to wind stimuli; action potentials were never observed at these resting potentials. However, when the 9DL interneurons were hyperpolarized to a membrane potential of approximately -60 mV, a single action potential at the leading edge of the wind stimulus response was sometimes observed.3.The wind stimulus threshold of the 9DL interneurons to the types of stimuli used in these studies was approximately 0.01 cm/s. Above this threshold, the excitatory responses increased logarithmically with increasing peak wind velocity up to approximately 0.5 cm/s.4.The 9DL interneurons were directionally sensitive; their response amplitudes varied with wind stimulus orientation. 9DL1 cells responded maximally when stimulated with wind directed at the front of the animal. The apparent peak in directional sensitivity of the 9DL2 interneurons varied between the side and the rear of the animal, depending upon the site of electrode penetration within the cells dendritic arbor.5.The locations of dendritic branches of the 9DL interneurons within the afferent map of wind direction were used to predict the excitatory receptive field of these interneurons.

Modeling frequency encoding in the cricket cercal sensory system

Abstract We constructed probabilistic models of afferent inputs and compartmental models of interneurons in the cricket cercal system to examine the effects of dendritic morphology, distribution of synaptic inputs, and membrane properties on interneuron directional tuning properties. The mean directional tuning of afferent inputs to an interneuron was an excellent predictor of its directional tuning. Location of the synapses on the interneurons’ dendrites was not essential to determining tuning characteristics, but had a substantial effect on sensitivity. Thus, we conclude that both sampling of the afferent population, and anatomical distribution of synaptic inputs are important determinants of an interneurons directional response.

Cylindrical Approximation of a Neuron from Reconstructed Polyhedron

Abstract The cercal sensory system of the cricket mediates the detection and analysis of low velocity air currents. Sensory stimuli are encoded as spatiotemporal patterns of activity within an afferent map that provides inputs to primary sensory interneurons. We have developed biophysically based interneuron models with synaptic inputs that are derived from a dynamic model of the afferent map activity. Using these models, we have studied the possible mechanisms for the frequency tuning of one type of interneuron in this system. Our results indicate that frequency preferences are primarily due to the passive electrotonic structure of the dendritic arbor and the dynamic sensitivity of the spike initiation zone.

Modeling ion channels from the cricket cercal sensory system

In this paper, we investigate the problem of approximating a neuron (which is a disconnected polyhedron P reconstructed from points sampled from the surface of a neuron) with minimal cylindrical segments. The problem is strongly NP-hard when we take sample points as input. We present a general algorithm which combines a method to identify critical vertices of P and useful user feedback to decompose P into desired components. For each decomposed component Q, we present an algorithm which tries to minimize the radius of the approximate enclosing cylindrical segment. Previously, this process can only be done manually by researchers in computational biology. Empirical results show that the algorithm is very efficient in practice.