Raymon M. Glantz

Visual Input and Motor Output of Command Interneurons of the Defense Reflex Pathway in the Crayfish

Visual systems hold a special fascination for a large number of neurophysiologists. This is due in part to the fact that the behavior of visual interneurons (INs) “more closely resembles perception than sensation” (Lettvin et al., 1959) and thus conveys the illusion that we are studying something that is very close to behavior. Some excellent illustrations of this point can be found in the studies of the optic nerve of the rock lobster by Wiersma and co-workers recently reviewed by York and Wiersma (1975).

Defense reflex and motion detector responsiveness to approaching targets: The motion detector trigger to the defense reflex pathway

SummaryThe latency of the crayfish,Procambarus clarki, visually evoked defense reflex varies inversely with the velocity of an approaching object (Figs. 3, 4, 5). Several lines of evidence demonstrate that the latency variations may be attributed to the time required for the target visual angle to expand by a criterion number of degrees (Table 1). The probability that a stimulus will elicit the defense reflex, increases monotonically with the velocity of target approach. Single unit analysis of optic nerve interneurons indicate that the sustaining unit response latency was ≧ reflex latency (Fig. 8). Dimming units were only weakly responsive to approaching objects. Furthermore, the dimming units exhibited very little differential responsiveness over 76% of the behaviorally relevant range of stimulus velocity (Fig. 10). Motion detectors exhibited strong responses to approaching targets (Fig. 11) and both the mean discharge rate and the number of brief interspike intervals/stimulus increased linearly with stimulus velocity (Fig. 14, 15). It is proposed that a central neuronal threshold for eliciting the defense reflex is a criterion number of motion detector spikes or brief interspike intervals.

Light input to crustacean neurosecretory cells

Electrical activity was recorded intracellularly from neurosecretory cells in the crayfish eyestalk identified by lucifer yellow injection. The activity is most commonly enhanced by illumination of retinal fields. Increments in spontaneous activity as well as bursts in otherwise silent cells were the most common type of response. Occasionally light-induced inhibitory responses were recorded. At neuropil level, light pulses result in EPSPs with amplitudes dependent on intensity of light and the previous adaptation to darkness.

Polarization sensitivity of crayfish photoreceptors is correlated with their termination sites in the lamina ganglionaris

Summary1.Crayfish,Procambarus clarkii, photoreceptor sensitivity to the e-vector of polarized light was measured with micropipettes filled with Lucifer Yellow. The terminals of the dye injected cells were located in the two plexiform layers of the lamina ganglionaris (first optic ganglion).2.Receptors with greater sensitivity to the horizontal e-vector orientation projected their terminals to the distal plexiform layer (epl1) (Fig. 2). Conversely, receptors with greater sensitivity to the vertical e-vector projected their terminals to the proximal plexiform layer (epl2) (Fig. 3).3.There was no spatial overlap in the locations of the two functional classes of receptor terminals (Fig. 4, Table 1). Thus monopolar cells with dendrites restricted to epl1 and epl2 (M3 and M4 of Nässel (1976) and Nässel and Waterman (1977)) can be unique information channels for horizontally and vertically polarized light respectively.

Intercellular dye migration and electrotonic coupling within neuronal networks of the crayfish brain

SummaryIntercellular dye migration (dye coupling) was studied in conjunction with functional indices of electrotonic coupling in 52 sensory interneurons of the brain and circumesophageal connectives of the crayfish,Procambarus clarkii. Dye-coupling was observed in 19 of the 52 successful injections. Dye-coupling between the symmetrically homologous medial giant neurons was observed in two out of three observations (Fig. 1). Dye-coupling was also observed between nongiant symmetrical homologues on five occasions and within clusters of morphologically similar cells on eight occasions. Seven of the preparations revealed coupling among three or more neurons (Figs. 4, 7; Table 1). In 18 of the 19 observations of dye-coupling, the dye was transferred exclusively from interneurons to other interneurons. The one exception was an interneuron to motoneuron transfer. In no instance was the dye transferred to a primary afferent. This is consistent with previous electrophysiological evidence indicating chemical synapses between primary afferents and interneurons. Dye-coupled cells also exhibited functional evidence consistent with the presence of electrotonic coupling among descending sensory interneurons: i) Two way excitatory transmission (Fig. 5); ii) Negligible transmission delay; iii) Synaptic potentials which follow presynaptic pulse trains at rates of up to 200 Hz and without attenuation (Fig. 6). It is concluded that a significant proportion of the descending interneurons are organized in electrotonically coupled networks of two to five morphologically similar neurons.

Visual adaptation: a case of nonlinear summation

Abstract The intensity-voltage ( I–V ) function of photoreceptors is known to be linear at low response levels and to saturate at higher levels. Both the increment threshold and dark adaptation are associated with steady-state signals upon which the threshold response is superimposed. The first derivative of the I–V function provides the gain at any steady-state signal level and thus determines the threshold.

Polarization sensitivity in crayfish lamina monopolar neurons

Abstract1.Polarization sensitivity (PS) was examined in photoreceptors and lamina monopolar cells (LMCs) in two species of crayfish, Procambarus clarkii and Pacifasticus leniusculus. The measurements were made with intracellular recordings and broad field illumination.2.PS is about 40% greater in Pacifasticus than in Procambarus (Table 1). In both species the LMC stationary PS profiles (estimated with flashes) are similar to those of receptors (Figs. 1 and 2). Both receptor and LMC sensitivity profiles are well described by cos2θ functions (Fig. 3). PS was observed in all receptors and 78% of LMCs.3.When stimulated with a rotating polarizer, receptors and LMCs exhibit membrane potential modulation with phase predicted by the stationary PS profile (Fig. 5). In photoreceptors, the polarization-elicited percent modulation falls off steeply as intensity increases. The LMC modulation is stronger than that in receptors and relatively insensitive to the mean intensity (Figs. 6 to 8). For low intensities the LMC modulation is 100%. The LMC dynamic behavior is consistent with either an opponency mechanism or strong but polarization-insensitive lateral inhibition.4.Receptors and LMCs exhibit steady-state differential sensitivity to stationary e-vector orientation (Fig. 9).5.About 10% of the LMC neurons exhibit PS maxima separated by 90°. These results imply a nonlinear summation of signals from orthogonal receptor channels (Fig. 10).

Polarization contrast and motion detection

Form and motion perception rely upon the visual system’s capacity to segment the visual scene based upon local differences in luminance or wavelength. It is not clear if polarization contrast is a sufficient basis for motion detection. Here we show that crayfish optomotor responses elicited by the motion of images derived from spatiotemporal variations in e-vector angles are comparable to contrast-elicited responses. Response magnitude increases with the difference in e-vector angles in adjacent segments of the scene and with the degree of polarization but the response is relatively insensitive to the absolute values of e-vector angles that compose the stimulus. The results indicate that polarization contrast can support visual motion detection.

The crayfish sustaining fibers

SummarySimultaneous intracellular and extracellular recordings were obtained from sustaining fibers (SFs) within the optic lobes of the crayfish compound eye.1.A step increase in illumination produces a large (∼ 25 mV) compound EPSP with an estimated reversal potential of −19 mV (Fig. 3). The visual responses are a significant fraction (∼50%) of the driving force. The time course and relative amplitudes of the transient and steady-state compound EPSP are similar to those of retinular cells.2.The SF integrating segment possesses linear I-Vm (Fig. 4) and I-FSPIKE (Fig. 5) characteristics which result in a linear VEPSP-FSPIKE function (Fig. 5) for responses to light stimuli. Thus, the transient SF discharge is a faithful reflection of its synaptic input.3.The profound adaptation of the SF discharge to rectangular pulses of illumination (Fig. 5) is primarily due to the adaptation of the SF spike generating mechanism. The steady-state compound EPSP is 83% of the peak transient voltage (Table 1). This implies that the pathway between retinular cells and SFs contains neurons capable of a high level of tonic response.4.No direct synaptic interactions have been observed among SFs. The observed spike crosscorrelations reported previously (Glantz and Nudelman 1976) are due to common presynaptic input. Periodic bursting during intense broad-field illumination is due to synchronization of this common excitatory input.5.Inhibition within the excitatory receptive field (Wiersma and Yamaguchi 1967; Glantz 1973) is expressed dramatically as a postexcitation depression, which results from a membrane hyperpolarization. The hyperpolarization appears to result in part from a direct postsynaptic inhibition of SFs.6.When these results are considered along with those reported previously, they indicate the important role that the SF,per se, plays in the determination of its visual properties, particularly its receptive field, response time course and linear input/ output characteristics.

The functional organization of the crayfish lamina ganglionaris

SummaryThe light responses of the second order lamina monopolar neurons were examined in the crayfish compound eye.1.Single cartridge monopolar neurons (M1–M4) (Fig. 2) exhibited nonspiking hyperpolarizing light responses; for M1; M3 and M4 the transient ‘on’ response operated over the same intensity range as the receptor, 3.5 log units (Fig. 3). M2 operated in a much narrower intensity range (1.5 log unit). The ‘on’ responses were associated with a 19% increase in conductance (Fig. 6).2.The hyperpolarizing ‘on’ response can be reversed at 18 mV below the resting membrane potential (Fig. 4).3.The half-angular sensitivity width of monopolar cells (in partially dark-adapted eyes) is 15°×8° (horizontal by vertical) (Fig. 5). Off axis stimuli elicit attenuated hyperpolarizing responses associated with a diminished conductance increase or depolarizing responses associated with a net decrease in conductance. The latter result is consistent with the presynaptic inhibition of a ‘background’ transmitter release which normally persists in the dark.4.Lateral inhibition is elicited from the area immediately surrounding the excitatory field, and it is associated with diminished transient responses and an accelerated decay of the response (Fig. 5). Inhibitory stimuli decrease the conductance change associated with the hyperpolarizing response (Fig. 7). The surround stimuli can also elicit depolarizing ‘off’ responses with reversal potentials positive to the membrane resting potential. It is concluded that the rapidly repolarizing monopolar cell response (Table 1) is modulated by both pre- and postsynaptic inhibitory mechanisms.5.A compartment model indicates that signal attenuation along a 500 μm length of monopolar cell axon is 22–34% (Fig. 8). Simulation of steady-state signal transmission suggests that passive (decremental) conduction is sufficient to convey 66 to 78% of the monopolar cell signal from lamina to medulla. The current-voltage relation in current clamp is linear over the physiological operating range, and there is no evidence for rectification (Fig. 6).6.Hyperpolarization of single monopolar cells (M1–M4) provides a polysynaptic excitatory signal to the medullary sustaining fibers (Fig. 9).