John K. Douglass

Conserved and Convergent Organization in the Optic Lobes of Insects and Isopods, with Reference to Other Crustacean Taxa

The shared organization of three optic lobe neuropils—the lamina, medulla, and lobula—linked by chiasmata has been used to support arguments that insects and malacostracans are sister groups. However, in certain insects, the lobula is accompanied by a tectum‐like fourth neuropil, the lobula plate, characterized by wide‐field tangential neurons and linked to the medulla by uncrossed axons. The identification of a lobula plate in an isopod crustacean raises the question of whether the lobula plate of insects and isopods evolved convergently or are derived from a common ancestor. This question is here investigated by comparisons of insect and crustacean optic lobes. The basal branchiopod crustacean Triops has only two visual neuropils and no optic chiasma. This finding contrasts with the phyllocarid Nebalia pugettensis, a basal malacostracan whose lamina is linked by a chiasma to a medulla that is linked by a second chiasma to a retinotopic outswelling of the lateral protocerebrum, called the protolobula. In Nebalia, uncrossed axons from the medulla supply a minute fourth optic neuropil. Eumalacostracan crustaceans also possess two deep neuropils, one receiving crossed axons, the other uncrossed axons. However, in primitive insects, there is no separate fourth optic neuropil. Malacostracans and insects also differ in that the insect medulla comprises two nested neuropils separated by a layer of axons, called the Cuccati bundle. Comparisons suggest that neuroarchitectures of the lamina and medulla distal to the Cuccati bundle are equivalent to the eumalacostracan lamina and entire medulla. The occurrence of a second optic chiasma and protolobula are suggested to be synapomorphic for a malacostracan/insect clade. J. Comp. Neurol. 467:150–172, 2003.

The computational basis of an identified neuronal circuit for elementary motion detection in dipterous insects.

Based on comparative anatomical studies and electrophysiological experiments, we have identified a conserved subset of neurons in the lamina, medulla, and lobula of dipterous insects that are involved in retinotopic visual motion direction selectivity. Working from the photoreceptors inward, this neuronal subset includes lamina amacrine (alpha) cells, lamina monopolar (L2) cells, the basket T-cell (T1 or beta), the transmedullary cell Tm1, and the T5 bushy T-cell. Two GABA-immunoreactive neurons, the transmedullary cell Tm9 and a local interneuron at the level of T5 dendrites, are also implicated in the motion computation. We suggest that these neurons comprise the small-field elementary motion detector circuits the outputs of which are integrated by wide-field lobula plate tangential cells. We show that a computational model based on the available data about these neurons is consistent with existing models of biological elementary motion detection, and present a comparable version of the Hassenstein-Reichardt (HR) correlation model. Further, by using the model to synthesize a generic tangential cell, we show that it can account for the responses of lobula plate tangential cells to a wide range of transient stimuli, including responses which cannot be predicted using the HR model. This computational model of elementary motion detection is the first which derives specifically from the functional organization of a subset of retinotopic neurons supplying the lobula plate. A key prediction of this model is that elementary motion detector circuits respond quite differently to small-field transient stimulation than do spatially integrated motion processing neurons as observed in the lobula plate. In addition, this model suggests that the retinotopic motion information provided to wide-field motion-sensitive cells in the lobula is derived from a less refined stage of processing than motion inputs to the lobula plate.

Functionally and Anatomically Segregated Visual Pathways in the Lobula Complex of a Calliphorid Fly

In dipteran insects, the lobula plate neuropil provides a major efferent supply to the premotor descending neurons that control stabilized flight. The lobula plate itself is supplied by two major parallel retinotopic pathways from the medulla: small‐field, magnocellular afferents that are implicated in achromatic motion processing and Y cells that connect the medulla with both the lobula plate and the lobula. A third pathway from the medulla involves transmedullary (Tm) neurons, which provide inputs to palisades of small‐field neurons in the lobula. Although, in their passage to the brain, many output neurons from the lobula plate are separated physically from their counterparts in the lobula, there is an additional class of lobula complex output neurons. This group is composed of retinotopic lobula plate‐lobula (LPL) and lobula‐lobula plate (LLP) cells, each of which has dendrites in both the lobula and the lobula plate. The present account describes the anatomy and physiology of exemplars of LPL and LLP neurons, a wide‐field tangential neuron that is intrinsic to the lobula complex, and representatives of the Tm‐ and Y‐cell pathways. We demonstrate novel features of the lobula plate, which previously has been known as a motion‐collating neuropil, and now also can be recognized as supporting direction‐ or nondirection‐specific responses to local motion, encoding of contrast frequency, and processing of local structural features of the visual panorama. J. Comp. Neurol. 396:84–104, 1998.

Retinotopic pathways providing motion-selective information to the lobula from peripheral elementary motion-detecting circuits

Recordings from afferent channels from the medulla supplying deep neuropils of the flys optic lobes reveal different filter properties among the three classes of afferent neurons: transmedullary cells, T2 neurons, and Y cells. Whereas transmedullary cells respond to local flicker stimuli without discriminating these from directional or oriented motion, the T2 afferent neurons show clear motion orientation selectivity, which corresponds closely with a morphological bias in the orientation of their dendrites and could also be influenced by systems of local recurrent neurons in the medulla. A Y cell having a clearly defined terminal in the lobula, but having dendrite‐like processes in the medulla and, possibly, the lobula plate, discriminates the direction of motion and its orientation. These results demonstrate unambiguously that the lobula receives information about motion and that the channels carrying it are distinct from those supplying wide‐field motion‐selective neurons in the lobula plate. Furthermore, recordings from a newly identified recurrent neuron linking the lobula back to the inner medulla demonstrate that the lobula discriminates nondirectional edge motion from flicker, thereby reflecting a property of this neuropil that is comparable with that of primary visual cortex in cats. The present findings support the proposal that elementary motion detecting circuits supply several parallel channels through the medulla, which segregate to, but are not shared by, the lobula and the lobula plate. The results are discussed in the context of other intracellular recordings from retinotopic neurons and with analogous findings from mammalian visual systems. J. Comp. Neurol. 457:326–344, 2003.

Pathways in Dipteran Insects for Early Visual Motion Processing

In insects, as in vertebrates, neuroanatomical, electrophysiological, and modelling studies have provided insights regarding identities and connections among neurones that accomplish elementary motion detection. These studies include intracellular recordings from identified wide-field neurones that collate local information about motion, intracellular recordings from identified, mainly non-spiking small-field neurones that are candidates for a cardinal role in motion detection, and comparative anatomical studies of retinotopic neurones that are evolutionarily conserved across taxa. Nevertheless, many important features of motion processing in insects have yet to be revealed. This review concentrates on two questions: what are the identities and relationships among neurones that participate in elementary motion detection? And, are there distinct functional classes of elementary motion detectors (EMDs) in insects?

Optic flow representation in the optic lobes of Diptera: modeling the role of T5 directional tuning properties

Abstract. An evolutionarily conserved system of small retinotopic neurons in dipteran insects, called bushy T-cells, provides information about directional motion to large collator neurons in the lobula plate. Physiological and anatomical features of these cells provide the basis for a model that is used to investigate requirements for generating optic flow selectivity in collators while allowing for evolutionary variations. This account focuses on the role of physiological tuning properties of T5 neurons. Various flow fields are defined as inputs to retinotopic arrays of T5 cells, the responses of which are mapped onto collators using innervation matrices that promote selectivity for flow type and position. Properties known or inferred from physiological and anatomical studies of neurons contributing to motion detection are incorporated into the model: broad tuning to local motion direction and the representation of each visual sampling unit by a quartet of small-field T5-like neurons with orthogonal preferred directions. The model predicts hitherto untested response properties of optic flow selective collators, and predicts that selectivity for a given flow field can be highly sensitive to perturbations in physiological properties of the motion detectors.

Optic flow representation in the optic lobes of Diptera: Modeling innervation matrices onto collators and their evolutionary implications

Abstract. A network model of optic flow processing, based on physiological and anatomical features of motion-processing neurons, is used to investigate the role of small-field motion detectors emulating T5 cells in producing optic flow selective properties in wide-field collator neurons. The imposition of different connectivities can mimic variations observed in comparative studies of lobula plate architecture across the Diptera. The results identify two features that are crucial for optic flow selectivity: the broadness of the spatial patterns of synaptic connections from motion detectors to collators, and the relative contributions of excitatory and inhibitory synaptic outputs. If these two aspects of the innervation matrix are balanced appropriately, the networks sensitivity to perturbations in physiological properties of the small-field motion detectors is dramatically reduced, suggesting that sensory systems can evolve robust mechanisms that do not rely upon precise control of network parameters. These results also suggest that alternative lobula plate architectures observed in insects are consistent in allowing optic flow selective properties in wide-field neurons. The implications for the evolution of optic flow selective neurons are discussed.

Diverse speed response properties of motion sensitive neurons in the fly’s optic lobe

Speed and acceleration are fundamental components of visual motion that animals can use to interpret the world. Behavioral studies have established that insects discriminate speed largely independently of contrast and spatial frequency, and physiological recordings suggest that a subset of premotor descending neurons is in this sense speed-selective. Neural substrates and mechanisms of speed selectivity in insects, however, are unknown. Using blow flies Phaenicia sericata, intracellular recordings and dye-fills were obtained from medulla and lobula complex neurons which, though not necessarily speed-selective themselves, are positioned to participate in circuits that produce speed-selectivity in descending neurons. Stimulation with sinusoidally varied grating motion (0–200°/s) provided a range of instantaneous velocities and accelerations. The resulting speed response profiles are indicative of four distinct speed ranges, supporting the hypothesis that the spatiotemporal tuning of mid-level neurons contains sufficient diversity to account for the emergence of speed selectivity at the descending neuron level. This type of mechanism has been proposed to explain speed discrimination in both insects and mammals, but has seemed less likely for insects due to possible constraints on small brains. Two additional recordings are suggestive of acceleration-selectivity, a potentially useful visual capability that is of uncertain functional significance for arthropods.