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

Abstract

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.

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

“…Our finding that response frequency but not response force strongly covaries with cue value shows that the former but not necessarily the latter factor needs to be taken into account when trying to link neural activity and cue value. In freely moving pigeons, many NCL neurons exhibit motor-related firing rate modulation 20 21 . Analyzing NCL firing rates relative to key pecks directed at the conditioned stimuli effectively factors out response frequency as a contributor to firing rate modulations, thus providing the opportunity to correlate response frequency (as an indicator of cue value) with neural firing rates largely untainted by sensorimotor contingencies of differential key pecking.…”

“…Several single-neuron recording studies have demonstrated that NCL neurons’ firing rates are strongly modulated during the presentation of reward-predicting visual stimuli 17 18 19 20 21 , during a post-stimulus delay phase preceding reward delivery 22 23 , and during the consumption of food and water rewards 17 18 19 20 24 . Possibly, activity in the delay (i.e.…”

Blocking NMDA-receptors in the pigeon’s “prefrontal” caudal nidopallium impairs appetitive extinction learning in a sign-tracking paradigm

“…The pigeon brain is devoid of a cerebral cortex, but their pallium is partly homologous to mammalian cortex. In addition, there is strong evidence that birds have a specialized pallial area, the nidopallium caudolaterale (NCL) which constitutes a functional equivalent to the mammalian PFC (reviewed in Güntürkün, 2005 ; Lengersdorf et al, 2014a ). Recently, Lengersdorf et al ( 2014b ) showed that transient NCL inactivation impairs context-specific extinction memory consolidation.…”

Does Early Environmental Complexity Influence Tyrosine Hydroxylase in the Chicken Hippocampus and “Prefrontal” Caudolateral Nidopallium?

“…The NCL is a specialized pallial area of the avian brain, which constitutes a functional equivalent to the mammalian prefrontal cortex ( 10 ) and has been shown to have a high density of NMDA receptors ( 12 ). The NCL is involved in decision making and learning ( 38 ) and pharmacological interventions such as the sodium channel blocker Tetrodotoxin and the NMDA receptor antagonist 2-amino-5-phosphonovalerianacid (APV) retard extinction learning ( 39 , 40 ). Like the mammalian prefrontal cortex, the NCL has a low density of D1 receptors ( 12 ).…”