Ralph A. DiCaprio

Proprioception in the first two joints of crustacean limbs is mediated by chordotonal organs that utilize spike-mediated information coding and transmission and by nonspiking proprioceptive afferents that use graded transmission at information rates in excess of 2,500 bits/s. Chordotonal organs operate in parallel with the graded receptors, but the information rates of the spiking chordotonal afferents have not been previously determined. Lower-bound estimates of chordotonal afferent information rates were calculated using stimulus reconstruction, which assumes linear encoding of the stimulus. The information rate was also directly estimated from the spike train entropy, which makes no a priori assumptions with respect to the coding scheme used by the system. Lower-bound information rate estimates ranged from 43 to 69 bits/s, whereas the direct estimates ranged from 24 to 278 bits/s. Comparison of both estimates derived from the same data set indicates that a linear decoder could recover an average of 59% of the information from the spike train. Afferent spike timing was found to be extremely precise, with spikes evoked with an average timing jitter of 0.55 ms. Information rate was correlated with the mean jitter and the noise entropy of the spike train could be predicted from the mean firing rate and mean jitter. Direct stimulation of single afferents by current injection into the soma revealed that the average timing jitter was <0.1 ms, indicating that intrinsic membrane properties, spike generation, and mechanotransduction mechanisms are the major sources of timing jitter in this system.

Although the role of the middle temporal (MT/V5) area and its medial superior temporal (MST) satellites in motion processing has been well explored, relatively little is known about motion regions located more rostrally in the superior temporal sulcus (STS), such as the fundus of the superior temporal (FST) area, the superior temporal polysensory (STP) region, or beyond. To fill this void, we used contrast-enhanced functional magnetic resonance imaging in awake macaques and a five-step testing procedure that allowed us to identify six motion-sensitive regions within the STS. Direction adaptation tests confirmed the motion sensitivity of these six regions. Five of them [MT/V5, its three satellites, and the middle part of the STP (STPm) region in the upper bank of the STS] have been documented by previous single-cell studies. A sixth, previously unknown motion-responsive region, which we termed the lower superior temporal (LST) region, was observed on the lower bank and fundus of the STS, 6–8 mm anterior to the FST area. In contrast to the MST areas, the LST region responds to slow as well as fast speeds and is responsive to static and moving images of objects, to patterns defined by opponent motion, and to actions. These results, obtained in both group and single-subject analyses, suggest that motion information in the STS might follow a second path, in addition to the MT/V5–MST path. This ventral path including the LST region, FST area, and STPm region is likely involved in the visual analysis of actions and biological motion.

The thoracic-coxal muscle receptor organ (TCMRO) is the only proprioceptor at the thoracic-coxal joint in the crab leg. The S and T afferent neurons of the TCMRO convey signals to the CNS solely by means of graded changes in membrane potential. The rate of information transfer of these afferents was determined by measuring the signal-to-noise ratio (SΝR) of these cells after repeated stimulation of the receptor with identical sequences of random movement and applying the Shannon formula for the information capacity of a Gaussian channel. Intracellular recordings were made from the S and T afferents adjacent to the transduction site at the origin of the receptor and along the axon 5–7 mm distal to this site. These nonspiking afferents transduce receptor movement and transmit this information with extremely high fidelity. The SNR of both neurons near the transduction site was >1000 over most of the 200 Hz stimulation bandwidth, and the mean information transfer rate was ∼2,500 bits/s. When calculated over a wider bandwidth of 500 Hz, the information rate was >4,600 bits/s. The effect of axonal cable properties on the information rate was evaluated by determining the SNR from membrane potential recordings made 5–7 mm distal to the transduction region. The major effect of graded transmission along the axon was attenuation and low-pass filtering of the sensory signal. The consequent reduction in signal power and bandwidth decreased the information transfer by ∼10–15% over 200 Hz and ∼30% over a 500 Hz bandwidth.

A general feature of motor patterns for locomotion is their cyclic and alternating organization. In walking, for example, rhythmic activity in leg motoneurons innervating antagonistic muscles of a joint is primarily antiphasic within each cycle. We investigate which role central pattern generating networks play in the generation of leg motoneuron activity in the absence of sensory feedback. We elicited activity in antagonistic flexor and extensor tibiae motoneurons in the deafferented mesothoracic ganglion of the stick insect by mechanically stimulating the head or abdomen, while recording intracellularly from their neuropilar processes. In most cases, tactile stimulation induced coactivation of tibial motoneurons. However, in ≈ 25% of the trials, tibial motoneurons generated alternating cycles consisting of bursts of action potentials that were terminated by strong inhibitory synaptic inputs. Injection of depolarizing current increased the amplitude of the inhibitory phase of the oscillation, while hyperpolarizing current decreased it and revealed a tonic depolarization of the motor neurons during the bout of rhythmic motor activity. The same results were gathered from recording tibial leg motoneurons during ‘twitching’ motor activity in decerebrated animals. Our results indicate that alternating rhythmic motoneuron activity in the deafferented stick insect walking system results from phasic inhibitory drive provided by central pattern generating networks. This inhibitory input patterns the firing of the motoneurons that results from a tonic depolarizing drive. This tonic depolarizing drive was also observed in tibial motoneurons of the deafferented mesothoracic ganglion during walking movements of the intact ipsilateral front leg.

The proprioceptors that signal the position and movement of the first two joints of crustacean legs provide an excellent system for comparison of spiking and nonspiking (graded) information transfer and processing in a simple motor system. The position, velocity, and acceleration of the first two joints of the crab leg are monitored by both nonspiking and spiking proprioceptors. The nonspiking thoracic-coxal muscle receptor organ (TCMRO) spans the TC joint, while the coxo-basal (CB) joint is monitored by the spiking CB chordotonal organ (CBCTO) and by nonspiking afferents arising from levator and depressor elastic strands. The response characteristics and nonlinear models of the input-output relationship for CB chordotonal afferents were determined using white noise analysis (Wiener kernel) methods. The first- and second-order Wiener kernels for each of the four response classes of CB chordotonal afferents (position, position-velocity, velocity, and acceleration) were calculated and the gain function for each receptor determined by taking the Fourier transform of the first-order kernel. In all cases, there was a good correspondence between the response of an afferent to deterministic stimulation (trapezoidal movement) and the best-fitting linear transfer function calculated from the first-order kernel. All afferents also had a nonlinear response component and second-order Wiener kernels were calculated for afferents of each response type. Models of afferent responses based on the first- and second-order kernels were able to predict the response of the afferents with an average accuracy of 86%.

Mechanosensory neurons exhibit a wide range of dynamic changes in response, including rapid and slow adaptation. In addition to mechanical factors, electrical processes may also contribute to sensory adaptation. We have investigated adaptation of afferent neurons in the stick insect femoral chordotonal organ (fCO). The fCO contains sensory neurons that respond to position, velocity, and acceleration of the tibia. We describe the influence of random mechanical stimulation of the fCO on the response of fCO afferent neurons. The activity of individual sensory neurons was recorded intracellularly from their axons in the main leg nerve. Most fCO afferents (93%) exhibited a marked decrease in response to trapezoidal stimuli following sustained white noise stimulation (bandwidth = 60 Hz, amplitudes from ±5 to ±30°). Concurrent decreases in the synaptic drive to leg motoneurons and interneurons were also observed. Electrical stimulation of spike activity in individual fCO afferents in the absence of mechanical stimulation also led to a dramatic decrease in response in 15 of 19 afferents tested. This indicated that electrical processes are involved in the regulation of the generator potential or encoding of action potentials and partially responsible for the decreased response of the afferents. Replacing Ca²⁺with Ba²⁺in the saline surrounding the fCO greatly reduced or blocked the decrease in response elicited by electrically induced activity or mechanical stimulation when compared with control responses. Our results indicate that activity of fCO sensory neurons strongly affects their sensitivity, most likely via Ca²⁺-dependent processes.

The motor neurons in the crab ventilatory system have previously been considered to be passive output elements in that the generation of bursts of action potentials in these neurons during ventilation was thought to be due to cyclic inhibition and excitation from the interneurons in the ventilatory central pattern generator. This study demonstrates that the large-amplitude depolarization that underlies bursts of action potentials in ventilatory motor neurons is produced by a plateau potential. These motor neurons satisfy a number of the experimental tests that have been proposed for plateau potentials, such as triggering of the burst by a brief depolarization, termination of the burst by a hyperpolarizing input, and an all-or-none suppression of the depolarizing potential by the injection of hyperpolarizing current.