Brain’s Response to Crucial Language Hub Removal: New Insights

Summary: A new study provides unprecedented insights into the human brain’s response to the loss of a key language hub.

During epilepsy surgery, the team recorded brain activity before and after the removal of the anterior temporal lobe, a hub for language meaning. These recordings revealed a rapid disruption in brain signaling and an attempt at partial compensation by distant brain areas, challenging previous theories about the replaceability of brain hubs.

This groundbreaking study offers new perspectives on the brain’s resilience and adaptability, and supports neurobiological theories about the brain’s tendency to maintain order.

Key Facts:

  1. The study was conducted during epilepsy surgery, allowing for unique pre- and post-operative brain recordings.
  2. The loss of the anterior temporal lobe caused immediate disruption in speech and language processing, followed by partial compensation by other brain areas.
  3. This research supports the theory that brain hubs are crucial for maintaining normal brain processing and that the brain actively works to regain order after hub loss.

Source: University of Iowa

A University of Iowa-led team of international neuroscientists have obtained the first direct recordings of the human brain in the minutes before and after a brain hub crucial for language meaning was surgically disconnected.

The results reveal the importance of brain hubs in neural networks and the remarkable way in which the human brain attempts to compensate when a hub is lost, with immediacy not previously observed. 

Hubs are critical for connectivity 

Hubs are everywhere. The hub of a bicycle wheel, with spokes shooting out from the center, keeps the wheel from collapsing when the bicycle is ridden. Airport hubs connect cities across the world. And social hubs like coffee shops or online social networks are places people gather for interaction. 

The human brain has hubs, too – the intersection of many neuronal pathways that help coordinate brain activity required for complex functions like understanding and responding to speech. However, whether highly interconnected brain hubs are irreplaceable for certain brain functions has been controversial.

By some accounts the brain, as an already highly interconnected neural network, can in principle immediately compensate for the loss of a hub, in the same way that traffic can be redirected around a blocked off city center.  

With a rare experimental opportunity, the UI neurosurgical and research teams led by Matthew Howard III, MD, professor and DEO of neurosurgery, and Christopher Petkov, PhD, professor and vice chair for research in neurosurgery, have achieved a breakthrough in understanding the necessity of a single hub.

By obtaining evidence for what happens when a hub required for language meaning is lost, the researchers showed both the intrinsic importance of the hub as well as the remarkable and rapid ability of the brain to adapt and at least partially attempt to immediately compensate for its loss.

The findings were reported recently in the journal Nature Communications.  

Evaluating the impact of losing a brain hub 

The study was conducted during surgical treatment of two patients with epilepsy. Both patients were undergoing procedures that required surgical removal of the anterior temporal lobe—a brain hub for language meaning—to allow the neurosurgeons access to a deeper brain area causing the patients’ debilitating epileptic seizures.

Before this type of surgery, neurosurgery teams often ask the patients to conduct speech and language tasks in the operating room as the team uses implanted electrodes to record activity from parts of the brain close to and distant from the planned surgery area.

These recordings help the clinical team effectively treat the seizures while limiting the impact of the surgery on the patient’s speech and language abilities.  

Typically, the recording electrodes are not needed after the surgical resection procedure and are removed. The innovation in this study was that the neurosurgery team was able to safely complete the procedure with the recording electrodes left in place or replaced to the same location after the procedure.

This made it possible to obtain rare pre- and post-operative recordings allowing the researchers to evaluate signals from brain areas far away from the hub, including speech and language areas distant from the surgery site.

Analysis of the change in responses to speech sounds before and after the loss of the hub revealed a rapid disruption of signaling and subsequent partial compensation of the broader brain network.  

“The rapid impact on the speech and language processing regions well removed from the surgical treatment site was surprising, but what was even more surprising was how the brain was working to compensate, albeit incompletely within this short timeframe,” says Petkov, who also holds an appointment at Newcastle University Medical School in the UK. 

The findings disprove theories challenging the necessity of specific brain hubs by showing that the hub was important to maintain normal brain processing in language. 

“Neurosurgical treatment and new technologies continue to improve the treatment options provided to patients,” says Howard, who also is a member of the Iowa Neuroscience Institute.

“Research such as this underscores the importance of safely obtaining and comparing electrical recordings pre and post operatively, particularly when a brain hub might be affected.”  

According to the researchers, the observation on the nature of the immediate impact on a neural network and its rapid attempt to compensate provides evidence in support of a brain theory proposed by Professor Karl Friston at University College London, which posits that any self-organizing system at equilibrium works towards orderliness by minimizing its free energy, a resistance of the universal tendency towards disorder.

These neurobiological results following human brain hub disconnection were consistent with several predictions of this and related neurobiological theories, showing how the brain works to try to regain order after the loss of one of its hubs.  

In addition to Petkov and Howard, the research team included researchers in the UI Departments of Neurosurgery, Radiology, and Psychological and Brain Sciences, as well as colleagues from Newcastle University, UCL, and University of Cambridge in the UK, and from Carnegie Mellon University, University of Wisconsin-Madison, and Gonzaga University in the United States. 

Funding: The research was funded in part by grants from National Institutes of Health, the Wellcome Trust. and the European Research Council. 

About this neuroplasticity research news

Author: Jennifer Brown
Source: University of Iowa
Contact: Jennifer Brown – University of Iowa
Image: The image is credited to Neuroscience News

Original Research: Open access.
Immediate neural impact and incomplete compensation after semantic hub disconnection” by Matthew Howard III et al. Nature Communications


Abstract

Immediate neural impact and incomplete compensation after semantic hub disconnection

The human brain extracts meaning using an extensive neural system for semantic knowledge. Whether broadly distributed systems depend on or can compensate after losing a highly interconnected hub is controversial.

We report intracranial recordings from two patients during a speech prediction task, obtained minutes before and after neurosurgical treatment requiring disconnection of the left anterior temporal lobe (ATL), a candidate semantic knowledge hub. Informed by modern diaschisis and predictive coding frameworks, we tested hypotheses ranging from solely neural network disruption to complete compensation by the indirectly affected language-related and speech-processing sites.

Immediately after ATL disconnection, we observed neurophysiological alterations in the recorded frontal and auditory sites, providing direct evidence for the importance of the ATL as a semantic hub.

We also obtained evidence for rapid, albeit incomplete, attempts at neural network compensation, with neural impact largely in the forms stipulated by the predictive coding framework, in specificity, and the modern diaschisis framework, more generally.

The overall results validate these frameworks and reveal an immediate impact and capability of the human brain to adjust after losing a brain hub.

Reference

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