Processing stages underlying word recognition in the anteroventral temporal lobe

Abstract

The anteroventral temporal lobe integrates visual, lexical, semantic and mnestic aspects of wordprocessing, through its reciprocal connections with the ventral visual stream, language areas, and the hippocampal formation. We used linear microelectrode arrays to probe population synaptic currents and neuronal firing in different cortical layers of the anteroventral temporal lobe, during semantic judgments with implicit priming, and overt word recognition. Since different extrinsic and associative inputs preferentially target different cortical layers, this method can help reveal the sequence and nature of local processing stages at a higher resolution than was previously possible.The initial response in inferotemporal and perirhinal cortices is a brief current sink beginning at 120ms, and peaking at ~170ms. Localization of this initial sink to middle layers suggests that it represents feedforward input from lower visual areas, and simultaneously increased firing implies that it represents excitatory synaptic currents. Until ~800ms, the main focus of transmembrane current sinks alternates between middle and superficial layers, with the superficial focus becoming increasingly dominant after ~550ms. Since superficial layers are the target of local and feedback associative inputs, this suggests an alternation in predominant synaptic input between feedforward and feedback modes. Word repetition does not affect the initial perirhinal and inferotemporal middle layer sink, but does decrease later activity. Entorhinal activity begins later (~200ms), with greater apparent excitatory postsynaptic currents and multiunit activity in neocortically-projecting than hippocampal-projecting layers. In contrast to perirhinal and entorhinal responses, entorhinal responses are larger to repeated words during memory retrieval.These results identify a sequence of physiological activation, beginning with a sharp activation from lower level visual areas carrying specific information to middle layers. This is followed by feedback and associative interactions involving upper cortical layers, which are abbreviated to repeated words. Following bottom-up and associative stages, top-down recollective processes may be driven by entorhinal cortex. Word processing involves a systematic sequence of fast feedforward information transfer from visual areas to anteroventral temporal cortex, followed by prolonged interactions of this feedforward information with local associations, and feedback mnestic information from the medial temporal lobe.

Bilateral Speech Comprehension Reflects Differential Sensitivity to Spectral and Temporal Features

“…The closest coupling of BOLD and comprehensibility changes appeared deep in the medial and anterior sections of the temporal lobe (Fig. 5A), regions supposedly involved in semantic retrieval processing (Devlin et al, 2002;Halgren et al, 2006). Another striking parallel was the increased efficacy of frequency spectrum: not only were spectral changes more powerful in driving the measured BOLD changes, they also yielded steeper changes in participants' comprehension ratings.…”

Left perirhinal cortex codes for similarity in meaning between written words: Comparison with auditory word input

“…Further evidence that perirhinal cortex plays a role in written word processing comes from invasive electrophysiological studies in humans (Nobre and McCarthy, 1995). Local field potential recordings, current source density analysis and single neuron recording in human perirhinal cortex indicate that during judgement of real-life size, familiarity or concreteness as well as during overt word recognition, written words evoke distinct effects in perirhinal cortex (Halgren et al, 2006;Chan et al, 2011). 4.4 No detectable semantic similarity effect for spoken word modality A priori we had expected that left perirhinal cortex would also exhibit a semantic similarity effect for the spoken word modality, in agreement with a putative role in amodal semantic processing. As mentioned above, in the Fairhall and Caramazza (2013) study RSA revealed semantic similarity effects for both written words and pictures in ventral temporal cortex, indicative for commonality at least between visual input modalities.…”

Laminar Population Analysis: Estimating Firing Rates and Evoked Synaptic Activity From Multielectrode Recordings in Rat Barrel Cortex

“…These studies are typically done on rat or cat in in vitro preparations. However, laminar-electrode recordings have been done in awake macaques (Schroeder et al 1998) and even humans (Halgren et al 2006;Ulbert et al 2001Ulbert et al , 2004Wang et al 2005). Thus LPA, combined with template-fitting analysis, offers opportunities for deeper insights into the functional synaptic connections even for these systems.…”