Deficits of hierarchical predictive coding in left spatial neglect

Author:

Doricchi Fabrizio12ORCID,Pinto Mario12,Pellegrino Michele12,Marson Fabio3,Aiello Marilena4,Campana Serena5,Tomaiuolo Francesco6ORCID,Lasaponara Stefano127

Affiliation:

1. Dipartimento di Psicologia 39, Sapienza Università di Roma, 00185 Roma, Italy

2. Laboratorio di Neuropsicologia dell’Attenzione, Fondazione Santa Lucia IRCCS, Neurorehabilitation Hospital, 00179 Roma, Italy

3. Fondazione Patrizio Paoletti—06081 Assisi, Perugia, Italy

4. Area of Neuroscience, SISSA, 34136 Trieste, Italy

5. Auxilium Vitae—Neurorehabilitation Hospital, 56048 Volterra (Pisa), Italy

6. Dipartimento di Medicina Clinica e Sperimentale, Università degli Studi di Messina, 98122 Messina, Italy

7. Dipartimento di Scienze Umane, Libera Università Maria Santissima Assunta—LUMSA, 00193 Roma, Italy

Abstract

Abstract Right brain-damaged patients with unilateral spatial neglect fail to explore the left side of space. Recent EEG and clinical evidence suggests that neglect patients might suffer deficits in predictive coding, i.e. in identifying and exploiting probabilistic associations among sensory stimuli in the environment. To gain direct insights on this issue, we focussed on the hierarchical components of predictive coding. We recorded EEG responses evoked by central, left-side or right-side tones that were presented at the end of sequences of four central tones. Left-side and right-side deviant tones produce a pre-attentive Mismatch Negativity that reflects a lower-order prediction error for the ‘Local’ deviation of the tone at the end of the sequence. Higher-order prediction errors for the frequency of these deviations in the acoustic environment, i.e. ‘Global’ deviation, are marked by the P3 response. We show that when neglect patients are immersed in an acoustic environment characterized by frequent left-side deviant tones, they display no pre-attentive Mismatch Negativity both for left-side deviant tones and infrequent omissions of the last tone, while they have Mismatch Negativity for infrequent right-side deviant tones. In the same condition, neglect patients show no P300 response to ‘Global’ prediction errors for deviant tones, including those in the non-neglected right-side, and omissions. In contrast to this, when right-side deviant tones are predominant in the acoustic environment, neglect patients have pre-attentive Mismatch Negativity both for right-side deviant tones and infrequent omissions, while they display no Mismatch Negativity for infrequent left-side deviant tones. Most importantly, in the same condition neglect patients show enhanced P300 response to infrequent left-side deviant tones, notwithstanding that these tones evoked no pre-attentive Mismatch Negativity. This latter finding indicates that ‘Global’ predictions are independent of ‘Local’ error signals provided by the Mismatch Negativity. These results qualify deficits of predictive coding in the spatial neglect syndrome and show that neglect patients base their predictive behaviour only on statistical regularities that are related to the frequent occurrence of sensory events on the right side of space.

Funder

Ministero della Ricerca Scientifica

Fondazione Santa Lucia

Publisher

Oxford University Press (OUP)

Subject

General Earth and Planetary Sciences,General Environmental Science

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