The role of the cerebral cortex in postural responses to externally induced perturbations

Highlights

• Rapid balance recovery responses are influenced by the cerebral cortex.

• Due to arousal, cortical processes can be hastened to contribute to the response.

• The cortex appears to covertly set the nervous system in advance to avoid falls.

• Effective balance responses in complex environments require cortical contributions.

Abstract

The ease with which we avoid falling down belies a highly sophisticated and distributed neural network for controlling reactions to maintain upright balance. Although historically these reactions were considered within the sub cortical domain, mounting evidence reveals a distributed network for postural control including a potentially important role for the cerebral cortex. Support for this cortical role comes from direct measurement associated with moments of induced instability as well as indirect links between cognitive task performance and balance recovery. The cerebral cortex appears to be directly involved in the control of rapid balance reactions but also setting the central nervous system in advance to optimize balance recovery reactions even when a future threat to stability is unexpected. In this review the growing body of evidence that now firmly supports a cortical role in the postural responses to externally induced perturbations is presented. Moreover, an updated framework is advanced to help understand how cortical contributions may influence our resistance to falls and on what timescale. The implications for future studies into the neural control of balance are discussed.

Introduction

A broadly distributed neural network controls upright stability in humans. While the relative contribution of distinct parts of the nervous system to maintain balance remains unclear it is now well established that even the most advanced regions of the neural hierarchy play some role in balance control. Most remarkable is the accumulating evidence that the cerebral cortex plays an important role in balance including compensatory reactions to unexpected postural challenge. This represents an important departure from the historical framework that placed postural regulation largely in the domain of subcortical networks.

A seemingly effortless ability to stay upright in healthy humans belies the sophisticated mechanisms acting to preserve an elevated centre of mass over a small bipedal base of support. However in many disease states, particularly those involving neurological disruption, the challenge of this task is exposed rendering numerous clinical populations vulnerable to falls. With significant societal and individual costs related to falls (e.g. severe injury and even death) this represents a major health care concern (Baker et al., 2011, Carroll et al., 2005, Kannus et al., 2005). Thus illuminating the underlying neural mechanisms for controlling balance is essential for developing targeted therapies to mitigate fall risk. As expected, considerable effort has gone into exploring factors that impact balance such as the role of different sensory cues in triggering corrective actions (Bolton and Misiaszek, 2009, Macpherson et al., 2007, Stapley et al., 2002) or spinal and brainstem mechanisms acting to stabilize the body (Bolton and Misiaszek, 2012, Honeycutt and Nichols, 2010, Macpherson and Fung, 1999, Mori, 1987). Conversely, much less research has investigated the role of the cerebral cortex in balance. This gap has likely been encouraged by the long-held belief that postural responses are mostly managed sub cortically (Magnus, 1926, Sherrington, 1910). Of course, this view has been reasonable given that reduced animal preparations retain an impressive capacity for generating complex righting reactions (Honeycutt and Nichols, 2010). Moreover, the comparably slow pace of sensory-cued voluntary acts versus the onset of automated postural responses has influenced the assumption that much of the neural processing related to generating balance reactions originates sub-cortically. While subcortical networks are critical in generating compensatory behaviour more recent investigations have demonstrated that the cerebral cortex makes a meaningful contribution to compensatory balance reactions.

The major shift towards recognising an important role for the cerebral cortex in balance control has been discussed previously (Jacobs and Horak, 2007, Maki and McIlroy, 2007) and the reader is referred to these comprehensive reviews. A critical distillation of these past reviews is that the cerebral cortex can: (1) Modulate upcoming potential postural responses via central set based on intention and knowledge of perturbation or environmental characteristics, (2) provide online monitoring of balance status and (3) modulate late-phase or change-in-support responses characteristics perhaps through direct control.

The present review extends upon past work to highlight some of the more recent advances. This includes updated information regarding cortical contributions to the perception (and prediction) of instability as well as a role in shaping the motor response. Where possible an indication of the impact of particular brain regions in responding to external perturbations will be provided. Moreover, compelling evidence now exists that postural threat is associated with accelerated engagement of cortical networks thus challenging previously assumed speed of transmission barriers to why the cerebral cortex could not play a role in rapid postural responses. This review will present the emerging evidence for a cortical role in reactive balance emphasizing research that directly measures cortical neurophysiology in association with externally induced postural responses. Moreover, suggestions for future research are provided. Overall, an updated framework is advanced for how the cerebral cortex may influence both the online generation of compensatory reactions as well as contributing to a priori setting of the central nervous system (CNS) state to influence such control.