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.

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

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.

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 network's 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.

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.

Visual motion-detection circuits in flies: parallel direction- and non-direction-sensitive pathways between the medulla and lobula plate.

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.

Visual motion detection circuits in flies: peripheral motion computation by identified small-field retinotopic neurons.

Giant motion-sensitive tangential neurons in the lobula plate are thought to be cardinal elements in the oculomotor pathways of flies. However, these large neurons do not themselves compute motion, and elementary motion detectors have been proposed only from theory. Here we identify the forms, projections, and responses of small-field retinotopic neurons that comprise a well known pathway from the retina to the lobula plate. Already at the level of the second and third synapses beneath the photoreceptor layer, certain of these small elements show responses that distinguish motion from flicker. At a level equivalent to the vertebrate inner plexiform layer (the fly's outer medulla) at least one retinotopic element is directionally selective. At the inner medulla, small retinotopic neurons with bushy dendrites extending through a few neighboring columns leave the inner medulla and supply inputs onto lobula plate tangentials. These medulla relays have directionally selective responses that are indistinguishable from those of large-field tangentials except for their amplitude and modulation with contrast frequency. Centrifugal neurons leading back from the inner medulla out to the lamina also show orientation-selective responses to motion. The results suggest that specific cell types between the lamina and inner medulla correspond to stages of the Hassenstein-Reichardt correlation model of motion detection.

Scotopic spectral sensitivity of the optomotor response in the green treefrog Hyla cinerea.

Amphibians are unusual among vertebrates in having two spectral classes of rod photoreceptors, unique amphibian "green" rods and typical vertebrate "red" rods. Although amphibians have been the subject of extensive research on visual function, it is not known whether possession of two classes of rods is a general feature of Amphibia, nor is it clear to what behaviors each class of rods contributes. The Hylidae comprise one of the largest families within Amphibia but have been little studied with respect to visual function. Here, we demonstrate the presence of green and red rods in Hyla cinerea by microspectrophotometry and provide evidence for the contribution of green rods to one visually based behavior, the optomotor response. In addition, we discuss the role of green and red rods in visually based behavior in light of apparently conflicting demands resulting from the need to maximize absolute sensitivity, visual acuity, and color sensitivity.

Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance.

In linear information theory, electrical engineering and neurobiology, random noise has traditionally been viewed as a detriment to information transmission. Stochastic resonance (SR) is a nonlinear, statistical dynamics whereby information flow in a multi-state system is enhanced by the presence of optimized, random noise. A major consequence of SR for signal reception is that it makes possible substantial improvements in the detection of weak periodic signals. Although SR has recently been demonstrated in several artificial physical systems, it may also occur naturally, and an intriguing possibility is that biological systems have evolved the capability to exploit SR by optimizing endogenous sources of noise. Sensory systems are an obvious place to look for SR, as they excel at detecting weak signals in a noisy environment. Here we demonstrate SR using external noise applied to crayfish mechanoreceptor cells. Our results show that individual neurons can provide a physiological substrate for SR in sensory systems.