Spatially Tuned Neurons in Corvid Nidopallium Caudolaterale Signal Target Position During Visual Search

Abstract

The avian pallial endbrain area nidopallium caudolaterale (NCL) shows important similarities to mammalian prefrontal cortex in connectivity, dopamine neurochemistry, and function. Neuronal processing in NCL has been studied with respect to sensory, cognitive, and reward information, but little is known about its role in more direct control of motor behavior. We investigated NCL activity during the choice period of a delayed match-to-sample task, as 2 trained crows searched and selected a previously remembered visual target among an array of 4 pictures. The crows exhibited behavioral response patterns consistent with serial visual search. Many single NCL neurons were spatially tuned to specific target positions during visual search and directed motor behavior. Moreover, single NCL neurons dynamically changed their tuning properties to represent different behaviorally relevant task variables across the trial. In consecutive task periods, single neurons responded to visual stimuli, stored stimulus information in working memory, guided goal-directed behavior depending on the remembered target picture, and encoded trial outcomes. This flexible encoding of all task-relevant aspects in the executive control of goal-directed behavior represents a striking convergence to neuronal encoding in primate prefrontal cortex. These data highlight key properties of associative endbrain areas underlying flexible cognitive behavior in corvids and primates.

Evolution of cognitive and neural solutions enabling numerosity judgements: lessons from primates and corvids

“…In the same way as the PFC, the NCL integrates highly processed sensory information for all modalities and projects to premotor structures, is modulated by dopamine, and interacts with limbic, visceral and memory-related structures. Recent single-unit recordings in behaving crows confirm the resemblance of the NCL with the PFC by showing that NCL neurons encode sensory and cognitive variables during working memory, but also participate in the translation of cognitive signals to motor behaviours [68,69]. As we shall see later, the NCL also plays an important role in numerical cognition.…”

Neurons in the pigeon caudolateral nidopallium differentiate Pavlovian conditioned stimuli but not their associated reward value in a sign-tracking paradigm

“…First, visual discrimination capacity is not impaired by either permanent lesion or transient inactivation of NCL 14 24 45 . Second, in working memory tasks, NCL-neurons are only weakly active during the actual stimulus presentation but increase their activity during the delay phase after stimulus offset in which the cue has to be kept in working memory 27 28 . Third, NCL neurons encode upcoming behavioral choices rather than current stimulus input during perceptual decision making 21 .…”

“…Possibly, activity in the delay (i.e. post-choice) phase represents a mixture of different processes like information about the relevant visual stimulus 25 , task-related rules 26 , reward expectancy 22 , and information about the upcoming behavioral choice 23 27 28 . The situation is less explored regarding initial (i.e.…”

Encoding of global visual motion in the nidopallium caudolaterale of behaving crows

“…When the crows chose the wrong motion direction, the encoding of the motion direction by the population of selective neurons was drastically reduced in error trials. This is in agreement with our previous findings for delayed response tasks: whenever the crows make errors, activity of selective NCL neurons is reduced and thus predictive of behavioural success (Veit & Nieder, ; Veit et al ., , ,b; Moll & Nieder, ). This suggests that sensory representations of NCL neurons are relevant to the birds’ behaviour on a trial‐by‐trial basis.…”