Stimulus-Response-Outcome Coding in the Pigeon Nidopallium Caudolaterale

Starosta, Sarah; Güntürkün, Onur; Stüttgen, Maik C.

doi:10.1371/journal.pone.0057407

Cited by 39 publications

(25 citation statements)

References 55 publications

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“…After training on the task, pigeons were implanted with custom-built microdrives (Bilkey & Muir, 1999;Bilkey, Russell, & Colombo, 2003;Starosta, G€ unt€ urk€ un, & St€ uttgen, 2013;Starosta, St€ uttgen, & G€ unt€ urk€ un, 2014) with seven electrodes made of 25 mm formvar coated nichrome wires (Science Products GmbH, Hofheim, Germany) and one additional 76 mm heavy polyimide coated stainless steel wire serving as reference (francoCorradi, Milano, Italy) that were connected to microconnectors (Omnetics Connector Corporation, Minneapolis, USA). All pigeons were implanted with one microdrive each in both the right and left hemisphere of the brain.…”

Section: Surgerymentioning

confidence: 99%

Categories in the pigeon brain: A reverse engineering approach

Koenen

Pusch

Bröker

et al. 2015

Jrnl Exper Analysis Behavior

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Pigeons are well known for their visual capabilities as well as their ability to categorize visual stimuli at both the basic and superordinate level. We adopt a reverse engineering approach to study categorization learning: Instead of training pigeons on predefined categories, we simply present stimuli and analyze neural output in search of categorical clustering on a solely neural level. We presented artificial stimuli, pictorial and grating stimuli, to pigeons without the need of any differential behavioral responding while recording from the nidopallium frontolaterale (NFL), a higher visual area in the avian brain. The pictorial stimuli differed in color and shape; the gratings differed in spatial frequency and amplitude. We computed representational dissimilarity matrices to reveal categorical clustering based on both neural data and pecking behavior. Based on neural output of the NFL, pictorial and grating stimuli were differentially represented in the brain. Pecking behavior showed a similar pattern, but to a lesser extent. A further subclustering within pictorial stimuli according to color and shape, and within gratings according to frequency and amplitude, was not present. Our study gives proof-of-concept that this reverse engineering approach-namely reading out categorical information from neural data--can be quite helpful in understanding the neural underpinnings of categorization learning.

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Section: Surgerymentioning

confidence: 99%

Categories in the pigeon brain: A reverse engineering approach

Koenen

Pusch

Bröker

et al. 2015

Jrnl Exper Analysis Behavior

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“…Whereas studies in head‐fixed pigeons found only very few neurons with motor‐related response modulation (Kalt et al ., ; Kirsch et al ., ), the present study and another recent study with freely moving pigeons (Starosta et al ., ) suggest that a much larger fraction of NCL neurons is involved in sensorimotor processing than previously thought. One explanation for the paucity of sensorimotor‐related activity found in head‐fixed preparations may be the limited range of movements that subjects could execute in that situation (using beak openings as operant responses).…”

Section: Discussionmentioning

confidence: 77%

“…Probably the most frequently found type of NCL neural response is that of either strong activation or suppression during reward presentation (Kalt et al ., ; Kirsch et al ., ; Koenen et al ., ; Starosta et al ., ). Indeed, 58/75 neurons in our sample significantly changed their activity during reward presentation.…”

Section: Resultsmentioning

confidence: 97%

“…First, a minor fraction of neurons (~20%) in both structures predicted choice direction before choice initiation; second, a major fraction of neurons (~70%) was modulated during the outcome period; and third, more neurons increased firing for negative outcomes [orbitofrontal cortex, reward omission; NCL, reward omission, punishment; also see Starosta et al . ()] than for positive outcomes (reward presentation).…”

Section: Discussionmentioning

confidence: 99%

“…The materials and recording procedures have been described in detail elsewhere (Starosta et al ., , ). Briefly, neural signals were picked up by eight formvar‐insulated nichrome wires (25 μm o.d., impedance ~0.5 MΩ) (Stablohm 675, California Fine Wire, Grover Beach, USA) connected to microplugs (Ginder Scientific, Nepean, CA, USA) housed in a custom‐built microdrive implant (Bilkey & Muir, ; Bilkey et al ., ), passed through a custom‐built headstage with unity gain, amplified 1000 × and bandpass‐filtered from 0.5 to 5 kHz online by a difference amplifier (DPA‐2FS, npi electronic GmbH, Germany), and digitised using an analog‐to‐digital converter (power 1401, Cambridge Electronic Design, Cambridge, UK) with sampling rates of 16–20 kHz.…”

Section: Methodsmentioning

confidence: 99%

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Neurons in the pigeon nidopallium caudolaterale signal the selection and execution of perceptual decisions

Lengersdorf¹,

Pusch²,

Güntürkün³

et al. 2014

Eur J of Neuroscience

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Sensory systems provide organisms with information on the current status of the environment, thus enabling adaptive behavior. The neural mechanisms by which sensory information is exploited for action selection are typically studied with mammalian subjects performing perceptual decision-making tasks, and most of what is known about these mechanisms at the single-neuron level is derived from cortical recordings in behaving monkeys. To explore the generality of neural mechanisms underlying perceptual decision making across species, we recorded single-neuron activity in the pigeon nidopallium caudolaterale (NCL), a non-laminated associative forebrain structure thought to be functionally equivalent to mammalian prefrontal cortex, while subjects performed a visual categorisation task. We found that, whereas the majority of NCL neurons unspecifically upregulated or downregulated activity during stimulus presentation, ~20% of neurons exhibited differential activity for the sample stimuli and predicted upcoming choices. Moreover, neural activity in these neurons was ramping up during stimulus presentation and remained elevated until a choice was initiated, a response pattern similar to that found in monkey prefrontal and parietal cortices in saccadic choice tasks. In addition, many NCL neurons coded for movement direction during choice execution and differentiated between choice outcomes (reward and punishment). Taken together, our results implicate the NCL in the selection and execution of operant responses, an interpretation resonating well with the results of previous lesion studies. The resemblance of the response patterns of NCL neurons to those observed in mammalian cortex suggests that, despite differing neural architectures, mechanisms for perceptual decision making are similar across classes of vertebrates.

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A comparative analysis of the dopaminergic innervation of the executive caudal nidopallium in pigeon, chicken, zebra finch, and carrion crow

Eugen

Tabrik

Güntürkün

et al. 2020

J of Comparative Neurology

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Despite the long, separate evolutionary history of birds and mammals, both lineages developed a rich behavioral repertoire of remarkably similar executive control generated by distinctly different brains. The seat for executive functioning in birds is the nidopallium caudolaterale (NCL) and the mammalian equivalent is known as the prefrontal cortex (PFC). Both are densely innervated by dopaminergic fibers, and are an integration center of sensory input and motor output. Whereas the variation of the PFC has been well documented in different mammalian orders, we know very little about the NCL across the avian clade. In order to investigate whether this structure adheres to species-specific variations, this study aimed to describe the trajectory of the NCL in pigeon, chicken, carrion crow and zebra finch. We employed immunohistochemistry to map dopaminergic innervation, and executed a Gallyas stain to visualize the dorsal arcopallial tract that runs between the NCL and the arcopallium. Our analysis showed that whereas the trajectory of the NCL in the chicken is highly comparable to the pigeon, the two Passeriformes show a strikingly different pattern. In both carrion crow and zebra finch, we identified four different subareas of high dopaminergic innervation that span the entire caudal forebrain. Based on their sensory input, motor output, and involvement in dopamine-related cognitive control of the delineated areas here, we propose that at least three morphologically different subareas constitute the NCL in these songbirds. Thus, our study shows that comparable to the PFC in mammals, the NCL in birds varies considerably across species.

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Stimulus-Response-Outcome Coding in the Pigeon Nidopallium Caudolaterale

Cited by 39 publications

References 55 publications

Categories in the pigeon brain: A reverse engineering approach

Categories in the pigeon brain: A reverse engineering approach

Neurons in the pigeon nidopallium caudolaterale signal the selection and execution of perceptual decisions

A comparative analysis of the dopaminergic innervation of the executive caudal nidopallium in pigeon, chicken, zebra finch, and carrion crow

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