Localized Brain Activation Related to the Strength of Auditory Learning in a Parrot

Parrots and songbirds learn their vocalizations from a conspecific tutor, much like human infants acquire spoken language. Parrots can learn human words and it has been suggested that they can use them to communicate with humans. The caudomedial pallium in the parrot brain is homologous with that of songbirds, and analogous to the human auditory association cortex, involved in speech processing. Here we investigated neuronal activation, measured as expression of the protein product of the immediate early gene ZENK, in relation to auditory learning in the budgerigar (Melopsittacus undulatus), a parrot. Budgerigar males successfully learned to discriminate two Japanese words spoken by another male conspecific. Re-exposure to the two discriminanda led to increased neuronal activation in the caudomedial pallium, but not in the hippocampus, compared to untrained birds that were exposed to the same words, or were not exposed to words. Neuronal activation in the caudomedial pallium of the experimental birds was correlated significantly and positively with the percentage of correct responses in the discrimination task. These results suggest that in a parrot, the caudomedial pallium is involved in auditory learning. Thus, in parrots, songbirds and humans, analogous brain regions may contain the neural substrate for auditory learning and memory

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Neuronal activation in the brain.

<p><b>A,B</b> Coronal sections of the budgerigar brain at the level of the dNCM and the hippocampus (A, cut at level “a” in D) and at the level of the vNCM and the CMM (B, cut at level “b” in D). Overlays represent the counting frames. Scale bar represents 1 mm. <b>C</b> Photomicrographs of coronal sections of the budgerigar brain showing Zenk immunoreactivity. Representative examples of Zenk-immunoreactive nuclei in the CMM (upper), the dNCM (middle), and the vNCM (lower) of birds that were trained and re-exposed to Japanese words (left), were not trained and exposed to Japanese words (middle), or kept in silence (right). Scale bar represents 50 µm. <b>D,E</b> Schematic diagrams of parasagittal views of the brains of avian vocal learners, parrots (D) and songbirds (E). Yellow regions indicate the caudomedial pallium, the NCM and the CMM. Ascending auditory pathways to Field L are similar in the two taxa (red arrows). Light grey regions indicate the vocal control system in parrots and the song system in songbirds. Lesion studies in adult and young songbirds led to the distinction between a caudal pathway (blue arrows), known as the song motor pathway (SMP), considered to be involved in the production of song, and a rostral pathway (blue dashed arrows), known as the anterior forebrain pathway (AFP), thought to play a role in song acquisition and auditory-vocal feedback processing. Equivalent pathways to the songbird SMP and AFP are proposed in the budgerigar <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0038803#pone.0038803-Jarvis4" target="_blank">[45]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0038803#pone.0038803-Brauth3" target="_blank">[79]</a>. Scale bar represents 1 mm. AAC, Central nucleus of anterior acropallium; APH, Parahippocampal area; Cb, Cerebellum; CLM, Caudal lateral mesopallium; CM, Caudal mesopallium; CMM, Caudomedial mesopallium; DLM, medial nucleus of dorsolateral thalamus; DMM, Magnocellular nucleus of the dorsomedial thalamus; HD, Densocellular part of the hyperpallium; HI, Intercalated part of the hyperpallium; HP, Hippocampus; HVC, acronym used as a proper name; L1, L2, L3, subdivisions of Field L complex; LaM, Mesopallial lamina; LMAN, Lateral magnocellular nucleus of the anterior nidopallium; LSt, Lateral striatum; MO, Oval nucleus of mesopallium; MStm, Magnocellular part of medial striatum; NAO, Oval nucleus of the anterior nidopallium; NC, Caudal nidopallium; dNCM, Dorsal part of the caudomedial nidopallium; vNCM, Ventral part of the caudomedial nidopallium; NF, Frontal nidopallium; NIVL, Ventral lateral nidopallium; NLC, Central nucleus of the lateral nidopallium; nXIIts, tracheosyringeal portion of the hypoglossal nucleus; RA, Robust nucleus of the acropallium.</p

Budgerigars can discriminate Japanese words.

<p><b>A</b> A schematic representation of the inside of the Skinner box. <b>B</b> Protocol of the go/no-go auditory discrimination task. <b>C</b> Sonagrams of the two Japanese words, spoken by a male budgerigar, used in the discrimination task. The top word means ‘hello’, and the bottom word means ‘have a nice day.’ <b>D</b> Mean proportion of correct responses in the go/no-go auditory discriminations. The mean (+ s.e.m.) percentage of correct responses for all of the trained birds over the first 5 sessions of training (100 trials per session) was not significantly above chance, but that over the last 5 sessions before stimulus re-exposure was significantly above chance (<i>n</i> = 7; ***<i>p</i><0.005).</p

Neuronal activation related to the strength of auditory learning.

<p><b>A</b> Mean (+ s.e.m.) number of Zenk-immunoreactive cells per square millimetre in the CMM, the NCM and the hippocampus for groups of male budgerigars in the Trained (<i>n</i> = 7), Untrained (<i>n</i> = 5) and Silence (<i>n</i> = 6) groups. Asterisks denote significant differences between the mean of the Trained group and the means of the two other groups (*<i>p</i><0.05, **<i>p</i><0.01). <b>B</b> Number of Zenk-immunoreactive cells per square millimetre in relation to the percentage correct responses in the discrimination task, in the CMM, the dNCM, the vNCM and the hippocampus. The correlation is significant in the CMM and the dNCM, but not in the vNCM or in the hippocampus.</p