Nonspatial and Subdivision-Specific Working Memory Deficits after Selective Lesions of the Avian Prefrontal Cortex

Abstract

Association areas in the avian forebrain are shown to subserve higher cognitive functions, including working memory. One of these areas, the neostriatum caudolaterale (NCL) of pigeons, has been functionally compared with the mammalian prefrontal cortex (PFC) because of its prominent role in spatial delay and reversal tasks and its innervation by the dopaminergic system that modulates these functions. However, whereas the PFC maintains in working memory information of different domains, the essential role of the NCL in working memory has been demonstrated only for spatial tasks. To investigate whether the avian NCL is also crucial for nonspatial working memory functions, pigeons were tested in an object-related (color) delayed matching-to-sample (DMTS) task. Bilateral lesions were placed in the entire, dorsal, or ventral NCL to test for possible functional subdivisions that were proposed to exist on the basis of neurochemical and behavioral data. Pigeons with total, dorsal, and ventral NCL lesions showed significant deficits in their DMTS performance, whereas controls were not impaired. Thus, the avian NCL is critically involved in nonspatial working memory processes. Recovery from performance deficits was observed in animals with ventral or total NCL lesions, whereas animals with dorsal NCL lesions showed no improvement. Ventral NCL may mediate perseverative behavior, whereas dorsal NCL might be involved in active working memory. Differences in the connections of these subdivisions with striatal areas and other association areas in the frontomedial forebrain underline functional differences. The data indicate a possible segregation of functions in the avian NCL.

Avian and mammalian “prefrontal cortices”: Limited degrees of freedom in the evolution of the neural mechanisms of goal-state maintenance

“…This similarity of PFC and NCL was first pointed out by Ivan Divac and coworkers [10,34]. Since then, numerous similarities at the behavioral, physiological, anatomical and biochemical level between NCL and PFC could be shown [7,8,24,28] (Fig. 1).…”

“…Since it is known that the prefrontal cortex of rodents seems to be especially tuned to spatial processes [36], it is important to clarify that the deficits in delayed alternation-tasks of NCL-lesioned pigeons are due to the memory and not due to the spatial component of this task. To this end, Diekamp et al [7] devised a matching-to-sample task that can not be coded in spatial terms and showed that NCL-lesions in pigeons resulted in working memory deficits. Additionally, the volume of tissue loss within NCL correlated significantly with memory loss within the task.…”

Neuro-economics in chicks: Foraging choices based on amount, delay and cost

“…Furthermore, tract tracing studies [13,51,53] revealed that AI has massive descending projections to the midbrain tegmentum and optic tectum, quite different from the mammalian amygdala. When viewed solely from a functional standpoint, AI might be a part of nidopallium -ventral pallium complex involved in the mnemonic and executive control [14,15,19,27]. It is required to develop a common set of tasks and experimental procedures, so the data obtained in different brain areas can be systematically compared.…”

“…A brief list of such outstanding case studies includes; object constancy in newly hatched domestic chicks [37], episodic-like memory in food-storing scrub jays [11], categorical discrimination of paintings by Picasso and Monet in pigeons [49] (also see [50] for Van Gogh and Chagall), possible insight of other individuals cognition [16], and verbal labeling and communication in grey parrots [33]. System neurophysiological studies on "prefrontal cortex" of pigeon cerebrum for working memory and executive control of behaviors [14,15,27] are also highly suggestive of the commonality.…”

Abstract rule neurons in the endbrain support intelligent behaviour in corvid songbirds

“…In pigeons, the nidopallium caudolaterale (NCL) of the endbrain has been identified as a key cognitive brain component, similar to the PFC in mammals 16 . Lesion and recording studies in pigeons demonstrated the NCL's importance for cognition (for example, working memory, reversal learning and reward prediction) [17][18][19][20][21] . Moreover, the two areas share important properties such as dense innervation by dopaminergic fibres and connectivity patterns with multiple sensory input, limbic and motor output regions 16 .…”