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Previous Article | Next Article
Volume 16, Number 15, Issue of August 1, 1996 pp. 4551-4562
Copyright ©1996 Society for NeuroscienceVisual Motion-Detection Circuits in Flies: Parallel Direction- and Non-Direction-Sensitive Pathways between the Medulla and Lobula Plate
John K. Douglass and Nicholas J. Strausfeld Arizona Research Laboratories, Division of Neurobiology, University of Arizona, Tucson, Arizona
ABSTRACT
The neural circuitry of motion processing in insects, as in primates, involves the segregation of different types of visual information into parallel retinotopic pathways that subsequently are reunited at higher levels. In insects, achromatic, motion-sensitive pathways to the lobula plate are separated from color-processing pathways to the lobula. Further parallel subdivisions of the retinotopic pathways to the lobula plate have been suggested from anatomical observations. Here, we provide direct physiological evidence that the two most prominent of these latter pathways are, indeed, functionally distinct: recordings from the retinotopic pathway defined by small-field bushy T-cells (T4) demonstrate only weak directional selectivity to motion, in striking contrast with previously demonstrated strong directional selectivity in the second, T5-cell, pathway. Additional intracellular recordings and anatomical descriptions have been obtained from other identified neurons that may be crucial in early motion detection and processing: a deep medulla amacrine cell that seems well suited to provide the lateral interactions among retinotopic elements required for motion detection; a unique class of Y-cells that provide small-field, directionally selective feedback from the lobula plate to the medulla; and a new heterolateral lobula plate tangential cell that collates directional, motion-sensitive inputs. These results add important new elements to the set of identified neurons that process motion information. The results suggest specific hypotheses regarding the neuronal substrates for motion-processing circuitry and corroborate behavioral studies in bees that predict distinct pathways for directional and nondirectional motion.
Key words: insects; vision; parallel pathways; motion processing; bushy T-cells; motion computation
INTRODUCTION
In flying insects, many behaviors rely upon visual motion information: gaze control (Hengstenberg, 1993), flight stabilization (Egelhaaf et al., 1988
Parallel pathways that process distinct features of sensory inputs are well known in visual systems. In insects (Strausfeld and Lee, 1991
Anatomical observations (Strausfeld, 1976
Fig. 1. Schematic view of parallel pathways to the lobula plate in the calliphorid fly brain (after Douglass and Strausfeld, 1995
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A major question in vision concerns the cellular nature of elementary motion detectors (EMDs). Theoretical arguments (Hassenstein and Reichardt, 1956
Until recently (Douglass and Strausfeld, 1995
MATERIALS AND METHODS
All experiments employed calliphorid flies, Phaenicia sericata, which are maintained as a laboratory colony at the Arizona Research Laboratories Division of Neurobiology. Eggs from locally trapped individuals were collected several times per year to help maintain the genetic diversity and fitness of the laboratory colony. As in a previous study (Douglass and Strausfeld, 1995Electrophysiological recordings. Intact male or female flies were immobilized with low-melting-point wax, with the head tilted downward at 45° from the horizontal axis. A small piece of cuticle was removed from behind the left or right brain to expose the medulla and lobula complex, and the brain was bathed in insect saline; all recordings were from the right brain, except for a medulla amacrine cell (see below). Borosilicate pipettes were filled with 4% Lucifer yellow in distilled water, backfilled with 0.1 M LiCl, and inserted into the rear surface of the optic lobe with a Leitz micromanipulator. Intracellular membrane voltages were monitored with standard AgCl electrodes and an intracellular amplifier (Neuroprobe 1600, AM Systems, Everett, WA) and recorded on a VCR with a Vetter 3000A PCM adapter (Rebersburg, PA). Intracellular voltages were recorded on the ``fast'' channel (25 µsec rise time), and photodiode records of stimulus parameters were monitored on additional channels (see below). Portions of the data were later replayed from tape or were digitized on-line and stored at 10 kHz on a PC (Datawave, Longmont, CO) for subsequent analysis. In situ pipette resistances ranged from ~70 to 140 M
. Small neurons occasionally were dye-filled unintentionally during brief penetrations. Measures taken to minimize the occurrence of multiple fills (Douglass and Strausfeld, 1995
Stimuli. Flies were positioned with the head at the center of the visual stimulus field, which was oriented parallel to the frontal plane of the head. All experiments were performed in a darkened room in a Faraday cage resting on a vibration isolation table (TMC, Peabody, MA). Impaled cells typically were stimulated first with square-wave grating motion and then with square-wave flicker, followed by additional motion or flicker stimuli when possible.
One recording from a deep amacrine cell (see Results) was obtained by using a stimulus arrangement fully described elsewhere (Douglass and Strausfeld, 1995
All other experiments employed computer-generated visual stimuli (Vision Research Graphics, Durham, NH) displayed on a high-resolution red-green-blue (rgb) monitor (Nanao 9080i, Japan). The 1024 × 512 pixel display was operated in rgb mode at a refresh rate of 117.3 Hz. This system permitted the presentation of a variety of stimuli in rapid succession, a major advantage for relatively short-lived intracellular recordings from very small neurons such as T4 and T5. Up to 15 precomputed stimulus objects at a time could be selected via keyboard input. At the start of each stimulus presentation, a 4 bit stimulus identification code was sent to a parallel port for recording on the VCR tape and the data acquisition PC. Precise stimulus-timing information was provided by two photodiodes (PIN 10DP, United Detector Technology, Hawthorne, CA), one of which monitored the full stimulus field, while the other monitored an image of the center of the field provided by a small mirror, lens, and circular aperture.
The 117 Hz refresh rate of the stimulus monitor is nearly twice that of a standard PC display. Although calliphorid fly photoreceptors and lamina monopolar cells are capable of responding to flicker rates well above 120 Hz, light-adapted response peaks lie below 30 Hz (French and Järvilehto, 1978
As the head of the fly was tilted downward during recordings, the stimulus CRT was also tilted downward and viewed via a first-surface mirror positioned directly below the head of the fly. The path length from the center of the CRT to the compound eyes was 31 cm, which provided a 50° horizontal by 40° vertical full-field view. Three basic types of square-wave stimuli were employed: a small-field, 4 Hz circular flicker stimulus (3.5 or 7° diameter), a circular window showing small-field grating motion in each of eight directions (3.5° diameter), and full-field grating motion in eight directions. The onscreen positions of small-field stimuli were controlled with a trackball. Both the small-field and wide-field gratings had a spatial frequency of 0.13 cpd. Whereas the small-field motion had a constant speed of 12°/sec (temporal frequency 4 Hz), wide-field motion speed was varied sinusoidally between 0 and 93°/sec (0-12 Hz). All stimuli were generated using fixed, equal intensity values for the three color guns (100 on a 0-255 scale); flicker ``Off'' and the grating trough intensities were set to 0, resulting in measured contrast ratios of >30. The mean intensity of full-field gratings at the position of the head of the fly was 2.5 lux, and the display background, used for small-field stimuli and during periods between stimulus presentations, was a uniform gray field ~0.6 log units below the maximum stimulus intensity.
Histology and anatomical reconstructions. Cells were stained with Lucifer yellow by applying a steady 1-2 nA hyperpolarizing current for up to 3 min. Brains were dissected away from the head capsules while immersed in fixative (4% Mallinkrodt formalin in Millonig's buffer, pH 7.2), and the retina and ommatidia were removed immediately to prevent the diffusion of fluorescent ommochrome pigments into the neural tissue. Brains were fixed for 1-2 hr at room temperature; some preparations were then fixed overnight at 4°C. Fixed tissue was rinsed twice in Millonig's buffer, dehydrated in an ethanol series followed by acetone, embedded in Spurr's (1969), and sectioned at 14 µm on a sliding microtome. Profiles of stained cells (optical sections) were scanned at 0.5-2 µm intervals with a confocal epifluorescence microscope (MRC 600, Bio-Rad, Richmond, CA). Confocal projections from separate plastic sections were merged with image-processing software (Corel Photopaint 4, Corel, Salinas, CA), assisted by observations of stereopairs of individual projections. Some preparations were also photographed on Kodak Ektachrome 400 or Fujichrome 1600 at 1 µm intervals with a Leitz Diaplan epifluorescence microscope. Reconstructions were drawn from projected photographs of conventional epifluorescence images or confocal images.
RESULTS
Intracellular recordings and Lucifer yellow injections were employed to investigate the morphologies and roles of small-field columnar inputs to the lobula plate (T4), wide-field projection and amacrine cells (H6, deep medulla amacrine), and centrifugal Y-cells (CY1 and CY2) in processing visual motion information. The recordings presented here illustrate some of the variety of nonspiking and spiking behaviors that are typical of many neurons involved in early visual processing in insects. None of the cells described in this report has, to our knowledge, been recorded from previously.A deep medulla amacrine with nondirectional responses
Figure 2 illustrates a wide-field amacrine cell that is intrinsic to the proximal medulla. This neuron may be homologous to a similar neuron named m:tan5 in the Syrphid fly, Eristalis tenax, which was believed to be an output tangential cell, but the location of the cell body was not determined (Strausfeld, 1970
Fig. 2. Intracellular recordings and anatomical reconstructions from a deep medulla amacrine. In A and B, top traces show intracellular voltage relative to the prestimulus baseline (O); bottom traces show the timing and duration of (A) flicker On and Off and (B) grating motion (arrows, motion direction). B, The middle trace records grating movements monitored at the center of the stimulus with a photodiode; vertical arrows illustrate the phase of grating motions relative to the intracellular responses. C, Confocal projections from four serial vertical sections through most of the medulla amacrine and reconstruction (bottom view) from the confocal projections. Ventral is to the left. Bracket indicates the T4 dendritic layer. The cell body lies within the chiasma between the medulla and the lobula complex. Magnification, 320×.
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In response to wide-field flicker (Fig. 2A), the deep medulla amacrine showed a transient 2-3 mV depolarization to Off and little or no On response. Responses to motion consisted of transient depolarizations at the temporal frequency of the grating. The receptive field characteristics of this neuron were not examined in detail. Stimulation with vertical motion in a 37° field, however (obtained with a circular aperture positioned within the focal plane of the grating), produced the largest amplitude responses at the center of the stimulus field and weaker responses in the periphery. These results are consistent with the anatomical position of this neuron in the most posterior region of the medulla and centered slightly ventral to the equator, which corresponds to medial retinotopic inputs shifted slightly dorsal to the equator of the compound eye. The timing of depolarizations relative to peaks in the photodetector record showed direction-dependent phase shifts, particularly during horizontal motion (Fig. 2B, vertical arrows). Such shifts, however, could arise from a slight difference between the receptive field of the cell and the position of the photodetector and therefore do not necessarily reflect a directionally selective response. In summary, the responses of this cell to flicker and motion are similar and show no clear evidence of directional motion information. Nevertheless, this neuron is in an ideal position to participate in elementary motion detection (see Discussion).
T4-cells are nondirectionally selective retinotopic inputs to the lobula plate
T4-cells are small-field retinotopic cells with finely branched dendritic trees along the proximal edge of the medulla and terminals usually restricted to one of the four directionally selective layers of the lobula plate. T4 and T5 neurons are indistinguishable at the light microscope level, except for the locations of their dendritic trees, respectively, in the proximal medulla and the outermost stratum of the lobula, facing the lobula plate (Fig. 1). In contrast to their morphological similarities, the physiological properties of T4- and T5-cells recorded thus far are strikingly different (see also Discussion). In short, T5-cells have fully developed directional selectivity characterized by excitatory and inhibitory responses to opposite motion directions, whereas T4 mainly exhibits depolarizations with very weak directional selectivity.Successful intracellular recordings and stainings have been obtained from two T4-cells. In the first experiment (Fig. 3A-C,G), there is no question as to the identity of the neuron, because only one stable recording was obtained, and a single T4-cell (Fig. 3C) was filled with dye. Sparse, distal dendritic extensions beyond the main body of the dendritic tree (Fig. 3C) have not been noted previously in calliphorid flies but easily could be missed in Golgi preparations. At present it is uncertain whether this feature is representative of T4 morphology. In the second preparation (Fig. 3D-F,G) a few brief penetrations were followed by a more stable recording that was continued for several minutes before application of a hyperpolarizing current for 4 min. Fluorescence microscopy revealed three stained cells: two T4 neurons within the same column and a third lightly stained neuron with its dendrites in the same column. Because one T4 neuron (Fig. 3F, 1) was by far the most brightly filled and the last impaled along the passage of the electrode, we conclude that this cell corresponds to the most stable recording. Both recorded T4-cells (Fig. 3A,D) responded to flicker with small, transient On depolarizations and very weak Off depolarizations. On depolarizations exhibited a latency of ~15 msec, and the On responses decayed within ~100 msec.
Fig. 3. Flicker and motion responses of T4-cells from two separate preparations. Data in A and B are from the T4 neuron illustrated in C; D, E, Data from T4 neuron 1 in F. In B and E, the top insets illustrate 800 msec periods from the corresponding bracketed regions below them. Bottom traces show grating velocity, which was varied sinusoidally from 0 to 12 Hz (0 to 93°/sec). C and F, Reconstructions merged from confocal projections (negative images). Solid arrows, T4 axons; arrowheads, cell body fibers. Open arrow in C, Occasional processes extending toward the more distal stratum occupied by deep medulla amacrines. In F, solid arrow 1 shows the site of pipette penetration into the T4 axon. G, Responses to 4-8 grating motion directions (p, progressive; r, regressive; u, upward; d, downward). Responses (filled circles, T4 in C; open circles, T4 1 in F) were measured as the mean voltage difference between the peak depolarization and subsequent repolarization during the first 10 cycles of grating motion. For the T4 neuron in C, the dotted circle shows the mean response level (n = 8 directions; data from the second recording are normalized to this mean), and arrowhead shows mean response angle (324.8°; vector length is negligible). Magnification in C and F, 970×.
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The responses of T4 to horizontal motion (Fig. 3B,E) and all other directions (data not shown) were also flicker-like, consisting of trains of small transient depolarizations during each cycle of grating motion. Despite this overall similarity to flicker responses, some subtle changes in activity clearly were related to motion direction. The amplitudes of the transient depolarizations were weakly but consistently direction-dependent, as illustrated for horizontal motion in Figure 3. In addition, the larger amplitude transient depolarizations were accompanied by a slow hyperpolarization that occurred between the trains of depolarizations (Fig. 3B,E). Overall response amplitudes were quantified for different motion directions by measuring the maximum intracellular voltage difference between the depolarizing phase and the subsequent repolarized-hyperpolarized phase. Despite the clear presence of directional information in the raw data, the response amplitudes (Fig. 3G) show no significant directional trend. This result is in stark contrast to the strongly directional responses of T5 neurons (Douglass and Strausfeld, 1995
It could be argued that directional responses may arise somewhere within T4 and could have been missed if the recordings were localized near the distal dendrites. The locus of pipette penetration, however, is visible in the confocal image of the second T4 as a hole near the end of the axon in the lobula plate (Fig. 3F, arrow 1). Additional arguments against a purely directional role for T4 neurons are considered in the Discussion.
Collation of directionally selective motion channels
H6 (Fig. 4) is a lobula plate tangential neuron that responds to directional motion (see below). Although the precise location of impalement could not be determined, the position of the pipette was in the lateral lobula plate. The dendritic field of H6 lies within the anterior, horizontally sensitive layer of the lobula plate (Buchner et al., 1984
Fig. 4. The wide-field lobula plate tangential cell H6. A, Reconstruction from confocal projections showing the junction of the cell body fiber with the axon (arrow, right inset). Oe, Oesophagus; Pl Deu, posterior lateral deutocerebrum. Left inset contrasts the absence of responses to a small-field (7°) flicker with the clear spiking responses to smaller-field (3.5°) motion. B, Time course of directionally selective responses to horizontal wide-field motion. C and D, Polar plots of directional selectivity measured in two ways (n = 2 trials at each motion direction). C, Differences in mean intracellular voltage 500 msec after and 50 msec before the start of motion in each direction; dotted circle shows the zero response level, representing no net change in intracellular voltage. D, Numbers of spikes during the initial 500 msec of motion (background activity was negligible). Mean response vectors (arrows) indicate the preferred directions for wide-field motion, which are similar whether responses are measured as voltage changes (C, 162.4°) or spike counts (D, 172.0°). Magnification in A, 160×; right inset, 360×.
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H6 exhibited robust spiking responses to motion and little background activity (~0.1 spikes/sec). This neuron appears to be more responsive to grating motion than to flicker, as indicated (Fig. 4A, left inset) by its clear spiking response to 3.5° motion (mean spike rate 6.4/sec in figure), and the lack of response (1.2 spikes/sec) to a larger (7°) flicker stimulus at the same location and having the same flux density. H6 was particularly sensitive, however, to wide-field motion (Fig. 4B). Regressive motion produced sustained spiking (62.5/sec) superimposed on a DC depolarization, whereas progressive motion resulted in a sustained hyperpolarization and completely inhibited the spiking. These responses were used to evaluate the directional selectivity of H6 to wide-field motion in two ways, as changes in average membrane voltage and in spiking activity during the first 500 msec of motion. Both measures (Fig. 4C,D) demonstrate strongest excitation during wide-field regressive motion directed slightly upward.
Additional, qualitative tests employing small-field (3.5°), regressive-upward grating motion suggested that the H6 receptive field includes a broad region of the ipsilateral visual field. Similarly, horizontal regressive motion of a single vertical bar (black or white on a gray background) produced strong spiking responses as long as the bar was moving within the ipsilateral visual field. The angular extent of these stimuli, however, was limited to the 40 × 50° view the fly had of the stimulus screen. On the basis of the dendritic morphology of H6, its full receptive field may encompass the entire ipsilateral visual field.
Centrifugal pathways from lobula plate to medulla
Y-cells (Strausfeld and Blest, 1970
Fig. 5. Confocal reconstructions and intracellular recordings from two centrifugal Y-cells filled intracellularly with Lucifer yellow. A, Horizontal projection of CY1, with posterior to right. B, Transverse projection of CY2, with dorsal at right. Dotted lines indicate individual retinotopic columns in the medulla (Me) and their corresponding projections (arrows) in the lobula plate (LoP) and lobula (Lo). C-F, Recordings from CY2. C, Flicker responses. Inset shows a peristimulus time histogram from the eight individual stimulus cycles. 60 Hz noise has been subtracted from this record (scale bar, 125 msec). D, E, Responses to horizontal and vertical motion, respectively. F, Changes in intracellular voltage measured as in Fig. 4C; mean response vector (arrow) = 45.2°. Magnification in A and B, 390×.
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A second species of centrifugal Y-cell is shown in Figure 5B. This neuron, termed CY2, has extensive tangential arborizations with numerous dendritic spines in the lobula plate. Terminals in the medulla are all proximal to the serpentine layer. The arborizations in the lobula plate occupy a small region that corresponds to frontomedial retinotopic inputs, in good agreement with qualitative tests of the receptive field for flicker. The lobula plate arborizations are split into two tangentially oriented layers, the first within the HS layer of the neuropil and the second in the VS layer and displaced dorsally by approximately five retinotopic columns. Thus, CY2 combines HS and VS inputs that are also retinotopically distinct. The axon bifurcates to penetrate the distal lobula and proximal medulla, arrayed tangentially and vertically in both cases through a range of approximately five columns. As in CY1, the projections of this cell into the medulla and lobula are varicose and sparsely branched, suggesting that these two components consist mainly of presynaptic terminals and that the lobula plate processes, which are spined, are the principal input region.
A comparison of the flicker latencies of CY2- and T4-cells is consistent with this conclusion. The responses of CY2 to a 7° diameter flicker stimulus (Fig. 5C) were transient depolarizations with variable timing during the On phase of the stimulus. A peristimulus time average of the illustrated flicker responses (Fig. 5C, inset; n = 8) shows a tendency for Off depolarizations to have larger amplitudes and shorter mean latencies (23.5 msec, measured to the start of depolarization) than the On depolarizations (mean latency 44.5 msec). The On latency is quite long, compared with a mean of 15.4 msec measured from T4-cells tested with the same stimulus (data from Fig. 3A,D; n = 8). Notwithstanding possible discrepancies in conduction times, such a large difference in flicker delays suggests that CY2 receives its main inputs at a higher level of processing than T4-cells.
CY2 showed tonic, nonspiking, directionally selective responses to motion. The strongest depolarizations were to progressive and upward motion, with somewhat weaker hyperpolarizations during regressive and downward motion (Fig. 5D,E). In addition to its directional selectivity, CY2 seems to be strongly influenced by the temporal properties of grating motion (contrast frequency or angular velocity). During progressive motion, the level of depolarization was positively correlated with stimulus speed (Fig. 5D). During upward motion, in contrast (Fig. 5E), depolarization levels were relatively stable except at higher speeds at which partial repolarizations were observed. Responses to progressive upward motion (data not shown) were approximately intermediate between these two patterns, showing fairly steady depolarization through most of the 0-12 Hz range of contrast frequencies tested. Although sinusoidally varying the motion speed provides a wealth of information within a short recording time, the responses to different motion speeds are not independent and should be interpreted with caution. Nevertheless, these results suggest a greater sensitivity to motion speed in CY2 than in either H6 or T4 neurons.
As in the analysis of H6 responses (Fig. 4C), the directional selectivity of CY2 was evaluated by computing the difference between the baseline membrane voltage and the mean voltage during the initial 500 msec of motion. Examination of the raw data suggested the presence of significant response latencies to motion, consistent with the relatively long flicker latencies noted above for this cell. Analyses performed over a range of possible response latencies (0-150 msec), however, showed no major effect on the overall pattern of directional selectivity. The polar plot in Figure 5F assumes a response latency of 38 msec, which is intermediate between the measured latencies to flicker On and Off. The mean response vector indicates a preference for combined progressive and upward motion in this neuron.
DISCUSSION
This paper describes intracellular recordings from identified neurons that, even based solely on their anatomical relationships within the optic lobe (Boscheck, 1971; Hausen, 1984Lobula plate tangential neurons collate but do not detect elementary motion
Because H6 shares certain characteristics with several other calliphorid lobula plate tangential cells, its designation as a new, uniquely identifiable cell requires careful justification. H6 has a large dendritic field in the lobula plate, terminal arborizations in the contralateral posterior slope of the brain, and directional selectivity to horizontal motion. This general description also fits H2-H5 (Hausen, 1984What, then, distinguishes H6 from H2? Although both cells share a similar morphology, are excited by regressive motion, and are inhibited by progressive motion, they nevertheless differ in important details. First, the H6 dendritic field fills the entire lobula plate (Fig. 4A), whereas in two independent reconstructions of H2 (Hausen, 1984
There is also evidence for physiological differences between these two neurons. H2 clearly demonstrates excitatory On and Off responses to stimulation with wide-field flicker (Strausfeld et al., 1995
Despite their morphological differences, the general functional role of H6 seems similar to that of H2, namely to report to the contralateral brain the presence of wide-field, regressive horizontal motion. What is the relative importance of spikes and graded potential changes in relaying directional information from H6 to its postsynaptic targets? Because of the distances involved and the fairly small axon diameter of H6, graded potential changes in the dendrites probably have no direct influence upon its postsynaptic targets, but they may contribute to the relatively narrow directional tuning of the spiking response (compare Fig. 4 C and D) by inhibiting spike generation during null direction motion.
Retinotopic, directionally selective feedback from the lobula plate
Lobula plate centrifugal Y neurons similar to the CY cells described here (Fig. 5) have been reported in Golgi preparations from Drosophila, in which dendrites in the lobula plate extend across all four directional layers, and terminals are restricted to the medullary strata proximal to the serpentine layer and to the outer lobula strata (Fischbach and Dittrich, 1989CY1 and CY2 neurons are intriguing from a computational standpoint because they may provide both feedback inputs to the proximal medulla and feed-forward to equivalent retinotopic locations in the lobula. The basic responses of CY2 to motion, noisy graded depolarizations or weak hyperpolarizations, are similar to responses of HS and VS neurons in the lobula plate. Significantly, the lobula plate arborizations are divided into two parts, one in the horizontal motion-sensitive layer and a second, retinotopically displaced, portion in the vertically sensitive layer. This arrangement, on a small scale, is analogous to the VH neuron and VS 1 neuron, both wide-field centripetal cells in the lobula plate that have bistratified dendritic fields and show hybrid physiological properties of HS and VS neurons (Eckert and Bishop, 1978
The deep medulla amacrine
The deep medulla amacrine is a newly identified neuron, possibly homologous to m:tan5 in the drone fly Eristalis tenax (Strausfeld, 1970This neuron exhibited transient depolarizations in response to flicker Off and during motion but with no clear directional component. Its layer relationships with other neurons suggest that this amacrine could be an essential part of elementary motion-detecting circuits. The arborizations just distal to the T4 dendritic layer are ideally situated for lateral connections among small-field retinotopic transmedullary neurons such as Tm1 (Strausfeld and Lee, 1991
The proposal that the deep medulla amacrine may participate in elementary motion detection suggests possible analogies with motion-detecting circuitry in vertebrates. In the rabbit, responses of directionally selective ganglion cells can be explained by a combination of the morphological asymmetry between starburst amacrine input and output connections (Famiglietti, 1983
Historical evidence that T4 processes directional motion
What functional role, if any, does T4 play in motion processing? Historically, anatomical and physiological evidence has favored a major role for both T4 and T5 in directional motion processing and has underpinned reasoned speculation that they themselves are components of EMDs (Hausen and Egelhaaf, 1989Evidence that T4 does not process directional motion
The first suggestion that T4 might not be directionally selective (Douglass and Strausfeld, 1995The present recordings strongly support the idea that T4 does not process directional motion, despite the paradoxical presence of weak directional signals in T4. If viewed in isolation from the robust directional selectivity of T5, one might interpret the weakly directional T4 signals as evidence of an early stage in elementary motion detection. However, because directional motion detection has already been accomplished at the Tm1 level or earlier (Douglass and Strausfeld, 1995
Fig. 6. Hypothetical circuit diagram yielding nondirectional, motion-specific outputs from inherently directional, correlation-type elementary motion detectors (EMDs). R, Receptor; L, first-order relay; X, connector between neighboring channels; D, delay or long-pass filter; M, integrator; O, second integrating stage that combines outputs of individual directionally selective EMDs to provide a nondirectional, motion-specific summation (compare Fig. 12 in Douglass and Strausfeld, 1995
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For any complete description of motion, both speed and direction must be evaluated. Behavioral experiments demonstrate that insects are capable of estimating both parameters, yet certain visually guided responses rely primarily on one parameter in isolation from the other. Optomotor responses clearly are tuned to directional cues, but the directional information is easily corrupted by changes in temporal frequency or spatial structure (Götz, 1965
FOOTNOTES
Received March 13, 1996; revised May 8, 1996; accepted May 9, 1996.
This work was funded by a grant from the National Center for Research Resources (RR08688).
We thank Carol Arakaki, Robert Gomez, and Charles Hedgecock for excellent technical assistance and several colleagues, including Elke Buschbeck and Drs. Yongsheng Li and Martina Wicklein, for stimulating discussions and suggestions on this manuscript.
Correspondence should be addressed to John K. Douglass, Arizona Research Laboratories Division of Neurobiology, 611 Gould-Simpson Building, University of Arizona, Tucson, AZ 85721.
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