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In 2001, she played Gertrude Temple, Shirley Temple's bad mother in the ABC television film Child Star: The Shirley Temple Story, based on Temple's 1988 autobiography.
In 2001, Britton also had a recurring role in the NBC political drama The West Wing in the third season, appearing in the two-part premiere titled "Manchester" and the sixth episode titled "Gone Quiet" as Connie Tate, a member of Bruno Gianelli's team.
She also appeared in the romantic comedy-drama No Looking Back (1998) and the mystery comedy-drama Looking for Kitty (2004), both directed by Edward Burns.
In 2001, she co-starred opposite Chris Eigeman and Jamie Harris in the romantic comedy The Next Big Thing.
Britton made her feature film debut in the independent comedy-drama film The Brothers Mc Mullen (1995), and the following year, she was cast as Nikki Faber on the ABC sitcom Spin City.
She later starred in the short-lived sitcoms The Fighting Fitzgeralds (2001) and Lost at Home (2003), and appeared in several films, most notably the sports drama film Friday Night Lights (2004) and the thriller film The Last Winter (2006).
For this role she was nominated for Primetime Emmy Award for Outstanding Lead Actress in a Miniseries or a Movie in 2012.
After leaving Spin City, Britton had a recurring role as Maggie Kimble Hume in the short-lived CBS crime drama The Fugitive.After The Brothers Mc Mullen, Britton was cast as Heather in a recurring role in the ABC sitcom Ellen, and starred as Cammie Barbash in the unsold Fox pilot Pins and Needles.In 1996, she began co-starring as Nikki Faber in the ABC sitcom Spin City opposite Michael J. Her character was written out of the show when Charlie Sheen replaced Fox.She played Vivien Harmon, who relocates with her family to California after a series of tragic marital and family issues.Unfortunately for The Harmons, the new house they purchase quickly reveals itself to be haunted.