Behaviorally Related Neural Plasticity in the Arthropod Optic Lobes

Astrada, Martín Berón de; Bengochea, Mercedes; Sztarker, Julieta; Delorenzi, Alejandro; Tomsic, Daniel

doi:10.1016/j.cub.2013.05.061

Cited by 28 publications

(38 citation statements)

References 35 publications

(57 reference statements)

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“…The latter circuit offers more opportunity for sensory adaptation. Support for this suggestion comes from physiological recordings in the crab optic-lobe columnar neurons showing adaptation during high-frequency stimulus repetitions, but presynaptic visual neurons responding consistently to the same stimuli (Berón de Astrada et al, 2013).…”

Section: Research Articlementioning

confidence: 98%

Responses ofDrosophilagiant descending neurons to visual and mechanical stimuli

Bacon

Ito

et al. 2014

Journal of Experimental Biology

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In Drosophila, the paired giant descending neurons (GDNs), also known as giant fibers, and the paired giant antennal mechanosensory descending neurons (GAMDNs), are supplied by visual and mechanosensory inputs. Both neurons have the largest cell bodies in the brain and both supply slender axons to the neck connective. The GDN axon thereafter widens to become the largest axon in the thoracic ganglia, supplying information to leg extensor and wing depressor muscles. The GAMDN axon remains slender, interacting with other descending neuron axons medially. GDN and GAMDN dendrites are partitioned to receive inputs from antennal mechanosensory afferents and inputs from the optic lobes. Although GDN anatomy has been well studied in Musca domestica, less is known about the Drosophila homolog, including electrophysiological responses to sensory stimuli. Here we provide detailed anatomical comparisons of the GDN and the GAMDN, characterizing their sensory inputs. The GDN showed responses to light-on and light-off stimuli, expanding stimuli that result in luminance decrease, mechanical stimulation of the antennae, and combined mechanical and visual stimulation. We show that ensembles of lobula columnar neurons (type Col A) and mechanosensory antennal afferents are likely responsible for these responses. The reluctance of the GDN to spike in response to stimulation confirms observations of the Musca GDN. That this reluctance may be a unique property of the GDN is suggested by comparisons with the GAMDN, in which action potentials are readily elicited by mechanical and visual stimuli. The results are discussed in the context of descending pathways involved in multimodal integration and escape responses.

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Section: Research Articlementioning

confidence: 98%

Responses ofDrosophilagiant descending neurons to visual and mechanical stimuli

Bacon

Ito

et al. 2014

Journal of Experimental Biology

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“…In fact, repeated ipsilateral visual stimulation at short intervals in these crabs induces changes that are specific to retinal position and are mediated by a subset of columnar neurons (Ber on de Astrada et al, 2013). We also know that LG neurons in each lobula of the crab are driven by both eyes, showing remarkably similar responses when stimulated by ipsilateral or contralateral visual stimuli Tomsic, 2004, 2008).…”

Section: Cell Morphology and Classesmentioning

confidence: 98%

“…Recent experiments using calcium-imaging techniques have proved that the rapid decline in the level of escape response produced by a high-frequency repetition of a visual danger stimulus can be explained by a change produced at the level of columnar elements presynaptic to the LGs (Ber on de Astrada et al, 2013). These were population recordings made at the lobula terminals of presumably transmedullary neurons.…”

Section: Indexing Terms: Arthropod; Crustacean; Insect; Transmedullarmentioning

confidence: 99%

Neural organization of the second optic neuropil, the medulla, in the highly visual semiterrestrial crab Neohelice granulata

Sztarker

Tomsic

2014

J of Comparative Neurology

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Crustaceans are widely distributed and inhabit very different niches. Many of them are highly visual animals. Nevertheless, the neural composition of crustacean optic neuropils deeper than the lamina is mostly unknown. In particular, semiterrestrial crabs possess a highly developed visual system and display conspicuous visually guided behaviors. A previous study shows that the first optic neuropil, the lamina of the crab Neohelice granulata, possesses a surprisingly high number of elements in each cartridge. Here, we present a comprehensive description of individual elements composing the medulla of that same species. Using Golgi impregnation, we characterized a wide variety of cells. Only considering the class of transmedullary neurons, we describe over 50 different morphologies including small- and large-field units. Among others, we describe a type of centrifugal neuron hitherto not identified in other crustaceans or insects that probably feeds back information to every cartridge in the medulla. The possible functional role of such centrifugal elements is discussed in connection with the physiological and behavioral information on visual processing available for this crab. Taken together, the results reveal a very dense and complex neuropil in which several channels of information processing would be acting in parallel. We further examine our results considering the similarities and differences found between the layered organization and components of this crustacean medulla and the medullae of insects.

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“…Although we deliberately only used competing objects of similar salience in this study, future studies using this paradigm could uncover whether SSVEP selectivity in the optic lobes is indeed predictive of any visual goal-directed behavior by, for example, determining whether it can be directed to an inherently less salient object (e.g., following a training session). This approach has recently been used to demonstrate plasticity in medulla cells in crabs following training (32) and could be the key to unraveling the predictive qualities of population-level responses of neurons in the medulla. In particular, because we know that attention in bees may be modulated by experience and different types of training (33)(34)(35), as has been observed in humans (36), in-depth studies of brain activity in walking bees navigating more complex environments or training regimes built into this paradigm could allow us to unravel the relationship between SSVEP activity in the optic lobes and learning and memory.…”

Section: Discussionmentioning

confidence: 99%

Selective attention in the honeybee optic lobes precedes behavioral choices

Paulk

Stacey

Pearson

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

109

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Attention allows animals to respond selectively to competing stimuli, enabling some stimuli to evoke a behavioral response while others are ignored. How the brain does this remains mysterious, although it is increasingly evident that even animals with the smallest brains display this capacity. For example, insects respond selectively to salient visual stimuli, but it is unknown where such selectivity occurs in the insect brain, or whether neural correlates of attention might predict the visual choices made by an insect. Here, we investigate neural correlates of visual attention in behaving honeybees (Apis mellifera). Using a closed-loop paradigm that allows tethered, walking bees to actively control visual objects in a virtual reality arena, we show that behavioral fixation increases neuronal responses to flickering, frequency-tagged stimuli. Attention-like effects were reduced in the optic lobes during replay of the same visual sequences, when bees were not able to control the visual displays. When bees were presented with competing frequency-tagged visual stimuli, selectivity in the medulla (an optic ganglion) preceded behavioral selection of a stimulus, suggesting that modulation of early visual processing centers precedes eventual behavioral choices made by these insects.invertebrate | vision | electrophysiology | local field potential A ttention allows animals to respond selectively to competing stimuli (1, 2). Stimulus-selective responses in the human brain can be endogenously driven, and this volitional form of attention has been referred to as a "top-down" process, to distinguish it from salience-driven or "bottom-up" attention (3). Although even insects display bottom-up attention (4-10), it is unclear whether attention-like selection in the insect brain might also precede or predict behavioral choices. The case for top-down attention is especially compelling for honeybees, which have welldemonstrated visual discrimination and cognitive capabilities (11)(12)(13)(14). To effectively relate attention processes to behavior, however, requires sophisticated behavioral tracking or recording brain activity from behaving insects selecting distinct objects (15). Previous psychophysical studies in insects have measured whole body movements using tethered, closed-loop flight paradigms (4-8, 15). However, most studies of visual perception and memory in the bee have involved free flight (11, 13, 14; but see ref. 16). To address the neural mechanisms subserving these behaviors, researchers have traditionally recorded brain activity from immobilized bees performing elemental associative learning (e.g., refs. 17 and 18). Animal immobilization, however, is not ideal for gaining a better understanding of the relationship between the complex cognitive behaviors seen in freely moving bees and the underlying neural activity (13,14). To this end, we developed a closed-loop paradigm for walking honey bees (19), allowing them to select and fixate visual cues by rotating an air-supported ball. To simultaneously examine attentio...

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Behaviorally Related Neural Plasticity in the Arthropod Optic Lobes

Cited by 28 publications

References 35 publications

Responses ofDrosophilagiant descending neurons to visual and mechanical stimuli

Responses ofDrosophilagiant descending neurons to visual and mechanical stimuli

Neural organization of the second optic neuropil, the medulla, in the highly visual semiterrestrial crab Neohelice granulata

Selective attention in the honeybee optic lobes precedes behavioral choices

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