Blocking NMDA-Receptors in the Pigeon’s Medial Striatum Impairs Extinction Acquisition and Induces a Motoric Disinhibition in an Appetitive Classical Conditioning Paradigm

Abstract

The medial striatum of birds resembles the mammalian dorsal striatum, which plays a key role in the extinction of learned behavior. To uncover the variant and invariant neural properties of extinction learning across species, we use pigeons as an animal model in an appetitive extinction paradigm. Here, we targeted a medial sub-region of the pigeon’s striatum that receives executive, visual and motor pallial projections. By locally antagonizing the N -methyl-D-aspartate (NMDA) receptors through 2-Amino-5-phosphonovalerianacid (APV) during extinction, we observed an unspecific disinhibition effect, namely an increase in conditioned pecking to a rewarded control stimulus. In addition, blocking the NMDA receptors substantially deteriorated the extinction acquisition, implying that the pigeons still responded vigorously to the CS- even without food reward during extinction. After correcting for the unspecific effect of APV, the impaired extinction acquisition remained significant, which leads to the assumption that the delayed extinction effect is possibly caused by deficits in the updating of value coding of altered reward contingencies. Also, the APV-induced disinhibition seems to result from local hyperactivity that primarily drives actions towards cues of high appetitive value. The overall correspondence of our results with those from mammals suggests common neural substrates of extinction and highlights the shared functionality of the avian and mammalian dorsal striatum despite 300 million years of independent evolution.

Beyond the classic extinction network: a wider, comparative view

“…TTX injections into NFL slow down extinction learning and reduce retrieval of context-specific extinction information. Notably, this effect is not due to perceptual impairment during learning (Gao et al, 2019a). Multiple projections fan out of NFL, and one of them leads to the hippocampus.…”

Dynamics Learning Rate Bias in Pigeons: Insights from Reinforcement Learning and Neural Correlates

“…The pigeon's head was fixed on a specially customized stereotaxic device, and then a small craniotomy was performed. According to the pigeon brain atlas [25,26], a 16-channel (4 × 4) microelectrode array was chronically implanted in the right striatal region (Figure 1c; AP 10.50 mm; ML ± 1.00 mm; DV 7.50 mm).…”

Molecular biology of serotonergic systems in avian brains

“…Regarding the nidopallium, previous studies have functionally associated it with the mammalian PFC, so few attempts have been made to associate the nidopallium with the mammalian amygdala ( Karten, 1997 , 2013 ; Güntürkün, 2005 ; Butler et al, 2011 ; Dugas-Ford et al, 2012 ; Herold et al, 2018 ). Although no previous studies using the Pavlovian fear conditioning paradigm have been conducted to examine the functions involved in the arcopallium and nidopallium, several studies using the pigeon appetite conditioning paradigm have been conducted to implicate parts of the arcopallium and nidopallium in extinction learning ( Lissek and Güntürkün, 2005 ; Lengersdorf et al, 2014 , 2015 ; Starosta et al, 2017 ; Gao et al, 2018 , 2019a , b ; Güntürkün et al, 2020 ). In avian, the medial and central amygdaloid structures and output projections from amygdala have been unveiled ( Abellán and Medina, 2009 ; Vicario et al, 2014 ; Hanics et al, 2017 ).…”