Stanley Heinze

Central neural coding of sky polarization in insects

Many animals rely on a sun compass for spatial orientation and long-range navigation. In addition to the Sun, insects also exploit the polarization pattern and chromatic gradient of the sky for estimating navigational directions. Analysis of polarization–vision pathways in locusts and crickets has shed first light on brain areas involved in sky compass orientation. Detection of sky polarization relies on specialized photoreceptor cells in a small dorsal rim area of the compound eye. Brain areas involved in polarization processing include parts of the lamina, medulla and lobula of the optic lobe and, in the central brain, the anterior optic tubercle, the lateral accessory lobe and the central complex. In the optic lobe, polarization sensitivity and contrast are enhanced through convergence and opponency. In the anterior optic tubercle, polarized-light signals are integrated with information on the chromatic contrast of the sky. Tubercle neurons combine responses to the UV/green contrast and e-vector orientation of the sky and compensate for diurnal changes of the celestial polarization pattern associated with changes in solar elevation. In the central complex, a topographic representation of e-vector tunings underlies the columnar organization and suggests that this brain area serves as an internal compass coding for spatial directions.

Sun compass integration of skylight cues in migratory monarch butterflies

Migrating monarch butterflies (Danaus plexippus) use a time-compensated sun compass to navigate from eastern North America to their overwintering grounds in central Mexico. Here we describe the neuronal layout of those aspects of the butterflys central complex likely to establish part of the internal sun compass and find them highly homologous to those of the desert locust. Intracellular recordings from neurons in the monarch sun compass network reveal responses tuned to specific E-vector angles of polarized light, as well as azimuth-dependent responses to unpolarized light, independent of spectral composition. The neural responses to these two stimuli in individual neurons are mediated through different regions of the compound eye. Moreover, these dual responses are integrated to create a consistent representation of skylight cues in the sun compass throughout the day. The results advance our understanding of how ambiguous sensory signals are processed by the brain to elicit a robust behavioral response.

Neuroarchitecture of the central complex of the desert locust: Intrinsic and columnar neurons

The central complex is a group of neuropils in the center of the insect brain. It consists of four major subunits: the upper and lower divisions of the central body (CBU, CBL), the protocerebral bridge (PB), and the paired noduli. A distinctive feature of the central complex is a modular architecture characterized by rows of 16 columns, intersected in the central body by stacks of layers. Evidence from locusts suggests that the central complex plays a major role in sky compass orientation. To understand signal processing in this brain area further, we have analyzed the morphologies of columnar neurons of the central complex of the locust Schistocerca gregaria. Intracellular dye fills revealed 21 types of columnar neurons that connect columns of different subunits, three types of pontine neurons linking pairs of columns within the CBU, and one amacrine cell. Most neurons appeared to be part of isomorphic sets with cell type‐specific heterolateral projection patterns. Evaluation of arborization areas and neuron polarity suggests that these neurons are either intrinsic to the central complex or provide output to the lateral accessory lobes (LALs) or anterior lip region. No direct connections were found between the CBU and CBL. Instead, neurons of either subdivision were connected with the PB, but projected to non‐overlapping regions in the LALs and to different layers of the noduli. This study provides novel insights into the functional organization of the central complex, especially with respect to its likely role in right‐left signal matching and decision making. J. Comp. Neurol. 511:454–478, 2008.

Transformation of polarized light information in the central complex of the locust.

Many insects perceive the E-vector orientation of polarized skylight and use it for compass navigation. In locusts, polarized light is detected by photoreceptors of the dorsal rim area of the eye. Polarized light signals from both eyes are integrated in the central complex (CC), a group of neuropils in the center of the brain. Thirteen types of CC neuron are sensitive to dorsally presented, polarized light (POL-neurons). These neurons interconnect the subdivisions of the CC, particularly the protocerebral bridge (PB), the upper and lower divisions of the central body (CBU, CBL), and the adjacent lateral accessory lobes (LALs). All POL-neurons show polarization-opponency, i.e., receive excitatory and inhibitory input at orthogonal E-vector orientations. To provide physiological evidence for the direction of information flow through the polarization vision network in the CC, we analyzed the functional properties of the different cell types through intracellular recordings. Tangential neurons of the CBL showed highest signal-to-noise ratio, received either ipsilateral polarized-light input only or, together with CL1 columnar neurons, had eccentric receptive fields. Bilateral polarized-light inputs with zenith-centered receptive fields were found in tangential neurons of the PB and in columnar neurons projecting to the LALs. Together with other physiological parameters, these data suggest a flow of information from the CBL (input) to the PB and from here to the LALs (output). This scheme is supported by anatomical data and suggests transformation of purely sensory E-vector coding at the CC input stage to position-invariant coding of 360°-compass directions at the output stage.

The Locust Standard Brain: A 3D Standard of the Central Complex as a Platform for Neural Network Analysis.

Many insects use the pattern of polarized light in the sky for spatial orientation and navigation. We have investigated the polarization vision system in the desert locust. To create a common platform for anatomical studies on polarization vision pathways, Kurylas et al. (2008) have generated a three-dimensional (3D) standard brain from confocal microscopy image stacks of 10 male brains, using two different standardization methods, the Iterative Shape Averaging (ISA) procedure and the Virtual Insect Brain (VIB) protocol. Comparison of both standardization methods showed that the VIB standard is ideal for comparative volume analysis of neuropils, whereas the ISA standard is the method of choice to analyze the morphology and connectivity of neurons. The central complex is a key processing stage for polarization information in the locust brain. To investigate neuronal connections between diverse central-complex neurons, we generated a higher-resolution standard atlas of the central complex and surrounding areas, using the ISA method based on brain sections from 20 individual central complexes. To explore the usefulness of this atlas, two central-complex neurons, a polarization-sensitive columnar neuron (type CPU1a) and a tangential neuron that is activated during flight, the giant fan-shaped (GFS) neuron, were reconstructed 3D from brain sections. To examine whether the GFS neuron is a candidate to contribute to synaptic input to the CPU1a neuron, we registered both neurons into the standardized central complex. Visualization of both neurons revealed a potential connection of the CPU1a and GFS neurons in layer II of the upper division of the central body.

Linking the Input to the Output: New Sets of Neurons Complement the Polarization Vision Network in the Locust Central Complex

Polarized light is a key feature of the blue sky, used by many animals as a sensory cue for compass navigation. Like other insects, locusts perceive the E-vector orientation of polarized light with a specialized region of their compound eye, the dorsal rim area. Neurons in the brain relay this information through several processing stages to the central complex. The central complex has a modular neuroarchitecture, composed of vertical columns and horizontal layers. Several types of central-complex neurons respond to dorsally presented, rotating E-vectors with tonic modulation of their firing frequency. These neurons were found at the input stage of the central complex, as well as near the proposed output stage, where neurons are tuned to form a compass-like representation of E-vector orientations underlying the columnar organization of the central complex. To identify neurons suited to link input and output elements, we recorded intracellularly from 45 neurons of the central complex. We report several novel types of polarization-sensitive neurons. One of these is suited to fill the gap between input and output stages of the central-complex polarization vision network. Three types of neurons were sensitive to polarized light in only 50% of experiments suggesting that they are recruited to the network depending on behavioral context. Finally, we identified two types of neurons suited to transfer information toward thoracic motor circuits. The data underscore the key role of two subunits of the central complex, the lower division of the central body and the protocerebral bridge, in sky compass orientation.

Anatomical basis of sun compass navigation II: The neuronal composition of the central complex of the monarch butterfly

Each fall, eastern North American monarch butterflies in their northern range undergo a long‐distance migration south to their overwintering grounds in Mexico. Migrants use a time‐compensated sun compass to determine directionality during the migration. This compass system uses information extracted from sun‐derived skylight cues that is compensated for time of day and ultimately transformed into the appropriate motor commands. The central complex (CX) is likely the site of the actual sun compass, because neurons in this brain region are tuned to specific skylight cues. To help illuminate the neural basis of sun compass navigation, we examined the neuronal composition of the CX and its associated brain regions. We generated a standardized version of the sun compass neuropils, providing reference volumes, as well as a common frame of reference for the registration of neuron morphologies. Volumetric comparisons between migratory and nonmigratory monarchs substantiated the proposed involvement of the CX and related brain areas in migratory behavior. Through registration of more than 55 neurons of 34 cell types, we were able to delineate the major input pathways to the CX, output pathways, and intrinsic neurons. Comparison of these neural elements with those of other species, especially the desert locust, revealed a surprising degree of conservation. From these interspecies data, we have established key components of a conserved core network of the CX, likely complemented by species‐specific neurons, which together may comprise the neural substrates underlying the computations performed by the CX. J. Comp. Neurol. 521:267–298, 2013.

Anatomical basis of sun compass navigation I: The general layout of the monarch butterfly brain.

Each fall, eastern North American monarch butterflies (Danaus plexippus) use a time‐compensated sun compass to migrate to their overwintering grounds in central Mexico. The sun compass mechanism involves the neural integration of skylight cues with timing information from circadian clocks to maintain a constant heading. The neuronal substrates for the necessary interactions between compass neurons in the central complex, a prominent structure of the central brain, and circadian clocks are largely unknown. To begin to unravel these neural substrates, we performed 3D reconstructions of all neuropils of the monarch brain based on anti‐synapsin labeling. Our work characterizes 21 well‐defined neuropils (19 paired, 2 unpaired), as well as all synaptic regions between the more classically defined neuropils. We also studied the internal organization of all major neuropils on brain sections, using immunocytochemical stainings against synapsin, serotonin, and γ‐aminobutyric acid. Special emphasis was placed on describing the neuroarchitecture of sun‐compass‐related brain regions and outlining their homologies to other migratory species. In addition to finding many general anatomical similarities to other insects, interspecies comparison also revealed several features that appear unique to the monarch brain. These distinctive features were especially apparent in the visual system and the mushroom body. Overall, we provide a comprehensive analysis of the brain anatomy of the monarch butterfly that will ultimately aid our understanding of the neuronal processes governing animal migration. J. Comp. Neurol. 520:1599–1628, 2012.

Integration of polarization and chromatic cues in the insect sky compass.

Animals relying on a celestial compass for spatial orientation may use the position of the sun, the chromatic or intensity gradient of the sky, the polarization pattern of the sky, or a combination of these cues as compass signals. Behavioral experiments in bees and ants, indeed, showed that direct sunlight and sky polarization play a role in sky compass orientation, but the relative importance of these cues are species-specific. Intracellular recordings from polarization-sensitive interneurons in the desert locust and monarch butterfly suggest that inputs from different eye regions, including polarized-light input through the dorsal rim area of the eye and chromatic/intensity gradient input from the main eye, are combined at the level of the medulla to create a robust compass signal. Conflicting input from the polarization and chromatic/intensity channel, resulting from eccentric receptive fields, is eliminated at the level of the anterior optic tubercle and central complex through internal compensation for changing solar elevations, which requires input from a circadian clock. Across several species, the central complex likely serves as an internal sky compass, combining E-vector information with other celestial cues. Descending neurons, likewise, respond both to zenithal polarization and to unpolarized cues in an azimuth-dependent way.

Unraveling navigational strategies in migratory insects

Long-distance migration is a strategy some animals use to survive a seasonally changing environment. To reach favorable grounds, migratory animals have evolved sophisticated navigational mechanisms that rely on a map and compasses. In migratory insects, the existence of a map sense (sense of position) remains poorly understood, but recent work has provided new insights into the mechanisms some compasses use for maintaining a constant bearing during long-distance navigation. The best-studied directional strategy relies on a time-compensated sun compass, used by diurnal insects, for which neural circuits have begun to be delineated. Yet, a growing body of evidence suggests that migratory insects may also rely on other compasses that use night sky cues or the Earths magnetic field. Those mechanisms are ripe for exploration.